Classical and augmentative biological control against ... - IOBC-WPRS

IOBC 

OILB 

WPRS 

SROP 

In te rn atio na l O rg an isatio n fo r B iolog ical an d In teg ra te d C on tro l o f N o xiou s 

A nim als a n d P lan ts: W e st Pa la ea rctic R e gio na l S e ctio n 

O rg an isatio n In te rn a tio n ale d e L utte B io lo giqu e e t In te g ré e con tre les A n im a ux et le s 

P la ntes N u isibles: S e ction R é gio na le O u est P a lé a rctiq ue 

Classical and augmentative biological 

control against diseases and pests: 

critical status analysis and review of factors 

influencing their success 

Edited by Philippe C. Nicot 

2011

The content of the contributions is the responsibility of the authors 

Published by the International Organization for Biological and Integrated Control of Noxious 

Animals and Plants, West Palaearctic Regional Section (IOBC/WPRS) 

Publié par l'Organisation Internationale de Lutte Biologique et Intégrée contre les Animaux 

et les Plantes Nuisibles, Section Ouest Palaéarctique (OILB/SROP) 

Copyright IOBC/WPRS 2011 

ISBN 978-92-9067-243-2 

Cover page photo credits: 

1and 3: M Ruocco, CNR 

2: Anderson Mancini 

4. P.C. Nicot, INRA 

1 

2 

3 

4

Preface 

One of the Research Activities (RA 4.3) of the European Network for Durable Exploitation of crop 

protection strategies (ENDURE * ) has brought together representatives of industry and scientists 

from several European countries with experience ranging from fundamental biology to applied field 

work on biological control against pests and diseases. The unique diversity of expertise and 

concerns allowed the group to set up very complementary approaches to tackle the issue of the 

factors of success of biocontrol. 

The initial part of the work accomplished by this group consisted in a thorough review of 

scientific literature published on all types of biological control. Although it had to be focused on 

selected key European crops and their major pests and pathogens, this review is unique in the scope 

of the topics it covered and in the comprehensive inventories it allowed to gather on the potential of 

biocontrol and factors of success at field level. 

In parallel with identifying knowledge gaps and key factors from published research, 

information was gathered on aspects linked to the production and commercialization of biocontrol 

agents. 

These results, complemented by the views of experts in the field of biocontrol consulted at the 

occasion of meetings of IOBC-wprs, allowed the identification of majors gaps in knowledge and 

bottlenecks for the successful deployment of biocontrol and lead to the proposition of key issues for 

future work by the research community, the field of development and prospects for technological 

improvement by industry. 

Avignon, June 2011 

Philippe C. Nicot 

* 

EU FR6 project 031499, funded in part by the European Commission 

i

Contributors 

ALABOUVETTE Claude, 

INRA, UMR1229, Microbiologie du Sol et de l'Environnement, 17 rue Sully, 

F-21000 Dijon, France 

Claude.Alabouvette@dijon.inra.fr 

current address: AGRENE, 47 rue Constant Pierrot 21000 DIJON, c.ala@agrene.fr 

BARDIN Marc, 

INRA, UR 407, Unité de Pathologie végétale, Domaine St Maurice, BP 94, 

F-84140 Montfavet, France 

Marc.Bardin@avignon.inra.fr 

BLUM Bernard, 

International Biocontrol Manufacturers Association, Blauenstrasse 57, 

CH-4054 Basel, Switzerland 

bjblum.ibma@bluewin.ch 

DELVAL Philippe, 

ACTA, Direction Scientifique, Technique et Internationale, 

ICB / VetAgroSup, 1 avenue Claude Bourgelat , F-69680 Marcy l'Etoile, France 

Philippe.Delval@acta.asso.fr 

GIORGINI Massimo, 

CNR, Istituto per la Protezione delle Piante, via Università 133, 

80055 Portici (NA), Italy 

giorgini@ipp.cnr.it 

HEILIG Ulf, 

IBMA, 6 rue de Seine, F-78230 Le Pecq, France 

ulf.heilig@cegetel.net 

KÖHL Jürgen, 

Wageningen UR, Plant Research International, Droevendaalsesteeg 1, 

P.O. Box 69, 6700 AB Wageningen, The Netherlands 

jurgen.kohl@wur.nl 

LANZUISE Stefania, 

UNINA, Dip. Arboricoltura, Botanica e Patologia Vegetale, 

Università di Napoli Federico II, via Università 100, 80055 Portici (NA), Italy 

ii

LORITO Matteo 



lorito@unina.it 

MALAUSA Jean Claude, 

INRA, UE 1254, Unité expérimentale de Lutte Biologique, 

Centre de recherche PACA, 400 route des Chappes, BP 167, 

F-06903 Sophia Antipolis, France 

Jean-Claude.Malausa@sophia.inra.fr 

NICOT Philippe C., 

INRA, UR 407, Unité de Pathologie végétale, Domaine St Maurice, BP 94, 

F-84140 Montfavet, France 

Philippe.Nicot@avignon.inra.fr 

RIS Nicolas, 

INRA, UE 1254, Unité expérimentale de Lutte Biologique, 

Centre de recherche PACA, 400 route des Chappes, BP 167, 

F-06903 Sophia Antipolis, France 

Nicolas.Ris@sophia.inra.fr 

RUOCCO Michelina, 



ruocco@ipp.cnr.it 

VINALE Francesco, 



frvinale@unina.it 

WOO Sheridan 



woo@unina.it 

iii

List of Tables 

Table 1: 

Table 2: 

Table 3: 

Table 4: 

Table 5: 

Table 6: 

Table 7: 

Table 8: 

Scientific papers published between 1973 and 2008 on biological control 

against major plant diseases (from CAB Abstracts® database). ..........................................2 

Numbers of references on biocontrol examined per group of disease/plant 

pathogen......................................................................................................................3 

Numbers of different biocontrol compounds and microbial species reported as 

having successful effect against key airborne pathogens/diseases of selected 

crops. ..........................................................................................................................4 

Microbial species of fungi/oomycetes, yeasts and bacteria reported to have a 

significant effect against five main types of airborne diseases or pathogens in 

laboratory conditions or in the field.................................................................................5 

References extracted from the CAB Abstracts database and examined for 

reviewing augmentation biological control in grapevine. .................................................13 

Biocontrol agents evaluated in researches on augmentative biological control 

of pests in grapevine. ..................................................................................................15 

Number of references on augmentative biocontrol agents per group and 

species of target pest in grapevine.................................................................................16 

Number of references reporting data on the efficacy of augmentative 

biocontrol of pests in grapevine. ...................................................................................18 

Table 9: Recent introductions of parasitoids as Classical Biocontrol agents ....................................31 

Table 10: 

Table 11: 

Consulted sources of information on authorized biocontrol plant protection 

products in five European countries: .............................................................................34 

Active substances suitable for biological control listed on Annex I of 

91/414/EEC (EU Pesticide Database) - Status on 21st April 2009.....................................36 

Table 12: Evidence for, and effectiveness of, induced resistance in plants by 

Trichoderma species (Harman et al., 2004a). .................................................................47 

Table 13: 

Table 14: 

Table 15: 

Table 16: 

Trichoderma-based preparations commercialized for biological control of 

plant diseases. ............................................................................................................49 

Compared structure of the production costs for a microbial biocontrol agent 

(MBCA) and a chemical insecticide (source IBMA). ......................................................59 

Compared potential costs of registration for a microbial biocontrol agent 

(MBCA) and a chemical pesticide (source IBMA)..........................................................60 

Compared estimated market potential for a microbial biocontrol agent 

(MBCA) and for a chemical pesticide (source: IBMA) ....................................................60 

iv

List of Tables (continued) 

Table 17: 

Table 18: 

Table 19: 

Table 20: 

Table 21: 

Compared margin structure estimates for the production and sales of a 

microbial biocontrol agent (MBCA) and a chemical pesticide (source IBMA)....................61 

Production systems selected for a survey of factors influencing biocontrol use 

in Europe (source IBMA) ............................................................................................63 

Geographical distribution of sampling sites for a survey of factors influencing 

biocontrol use in Europe (source IBMA) .......................................................................63 

Structure of the questionnaire used in a survey of European farmers and 

retailers of biological control products...........................................................................64 

Impact of twelve factors on the future use of biocontrol agents by European 

farmers according to a survey of 320 farmers .................................................................66 

v

List of Figures 

Figure 1: 

Figure 2: 

Evolution of the yearly number of publications dedicated to biological control 

of plant diseases based on a survey of the CAB Abstracts® database. .................................1 

Range of efficacy of 157 microbial biocontrol agents against five main types 

of airborne diseases. Detailed data are presented in Table 4.............................................10 

Figure 3: Number of papers per year published during 1998-2008 concerning 

augmentative biological control of pests in grapevine......................................................13 

Figure 4: 

Figure 5: 

Figure 6: 

Figure 7: 

Figure 8: 

Figure 9: 

Figure 10: 

Figure 11: 

Figure 12: 

Groups of biocontrol agents investigated in augmentative biological control 

researches in grapevine. Number of references for each group is reported..........................19 

Groups of target pests investigated in augmentative biological control 

researches in grapevine. Number of references for each group is reported..........................19 

Large-scale temporal survey of the publications associated with classical 

biological control........................................................................................................26 

Relative importance of the different types of biocontrol during the temporal 

frame [1999-2008]......................................................................................................27 

Number of pest species and related citation rate by orders during the period 

[1999 ; 2008] .............................................................................................................28 

Relationships between the number of publications associated to the main 

pests and the relative percentage of ClBC related studies.................................................29 

Frequencies of papers and associated median IF related to the different 

categories of work ......................................................................................................30 

Estimated sales of biocontrol products in Europe in 2008 (in Million €). The 

estimates were obtained by extrapolating use patterns in a representative 

sample of EU farmers..................................................................................................64 

Estimated distribution of biocontrol use among types of crops in 2008 in 

Europe ......................................................................................................................65 

vi

Contents 

Chapter 1 

Potential of biological control based on published research. 

1. Protection against plant pathogens of selected crops...................................................1 

P. C. Nicot, M. Bardin, C. Alabouvette, J. Köhl and M. Ruocco 

Chapter 2 


2. Beneficials for augmentative biocontrol against insect pests. The 

grapevine case study .......................................................................................................12 

M. Giorgini 

Chapter 3 


3. Research and development in classical biological control with 

emphasis on the recent introduction of insect parasitoids .......................................20 

N. Ris and J.C. Malausa 

Chapter 4 

Registered Biocontrol Products and their use in Europe...................................................34 

U. Heilig, P. Delval and B. Blum 

Chapter 5 

Identified difficulties and conditions for field success of biocontrol. 

1. Regulatory aspects ................................................................................................. 42 

U. Heilig, C. Alabouvette and B.Blum 

Chapter 6 


2. Technical aspects: factors of efficacy ...........................................................................45 

M. Ruocco, S. Woo, F. Vinale, S. Lanzuise and M. Lorito 

Chapter 7 


3. Economic aspects: cost analysis ....................................................................................58 

B. Blum, P.C. Nicot, J. Köhl and M. Ruocco 

Chapter 8 


4. Socio-economic aspects: market analysis and outlook ..............................................62 

B. Blum, P.C. Nicot, J. Köhl and M. Ruocco 

Conclusions and perspectives 

Perspectives for future research-and-development projects on biological 

control of plant pests and diseases.................................................................................. 68 

P.C. Nicot, B. Blum, J. Köhl and M. Ruocco 

vii

Appendices....................................................................................................................... 71 

For Chapter 1 

Appendix 1. 

Appendix 2. 

Appendix 3. 

Appendix 4. 

Appendix 5. 

Inventory of biocontrol agents described in primary literature 

(1998-2008) for successful effect against Botrytis sp. in laboratory 

experiments and field trials with selected crops ...........................................72 


(1998-2008) for successful effect against powdery mildew in 

laboratory experiments and field trials with selected crops. .......................102 


(1973-2008) for successful effect against the rust pathogens in 

laboratory experiments and field trials with selected crops.........................111 


(1973-2008) for successful effect against the downy mildew / late 

blight pathogens in laboratory experiments and field trials with 

selected crops............................................................................................115 


(1973-2008) for successful effect against Monilinia in laboratory 

experiments and field trials with selected crops .........................................122 

Appendix 6. Primary literature (2007-2009) on biological control against 

Fusarium oxysporum.................................................................................128 

For Chapter 2 

Appendix 7. 

Appendix 8. 

Number of references retrieved by using the CAB Abstracts 

database in order to review scientific literatures on augmentative 

biological control in selected crops for Chapter 2. .....................................139 

Collection of data on augmentative biological control of pests in 

grapevine. Each table refers to a group of biocontrol agents.......................141 

For Chapter 3 

Appendix 9. 

References on classical biological control against insect pests 

(cited in Chapter 3)....................................................................................152 

For Chapter 4 

Appendix 10. Substances included in the "EU Pesticides Database" as of April 21 

2009..........................................................................................................163 

Appendix 11. 

Invertebrate beneficials available as biological control agents 

against invertebrate pests in five European countries. ................................171 

viii

Chapter 1 


1. Protection against plant pathogens of selected crops 

Philippe C. Nicot 1 , Marc Bardin 1 , Claude Alabouvette 2 , Jürgen Köhl 3 and Michelina Ruocco 4 

1 INRA, UR407, Unité de Pathologie Végétale, Domaine St Maurice, 84140 Montfavet, France 

2 INRA, UMR1229, Microbiologie du Sol et de l'Environnement, 17 rue Sully, 21000 Dijon, France 

3 Wageningen UR, Plant Research International, Droevendaalsesteeg 1, P.O. Box 69, 6700 AB 

Wageningen, The Netherlands 

4 CNR-IPP, Istituto pel la Protezione delle Piante, Via Univrsità 133, Portici (NA) Italy 

Evolution of the scientific literature 

The scientific literature published between 1973 and 2008 comprises a wealth of studies on 

biological control against diseases and pests of agricultural crops. A survey of the CAB Abstracts® 

database shows a steady increase in the yearly number of these publications from 20 in 1973 to over 

700 per year since 2004 (Figure 1). 

900 

Number of publications per year 

800 

700 

600 

500 

400 

300 

200 

100 

0 

1970 1975 1980 1985 1990 1995 2000 2005 2010 

Publication year 

Figure 1: 

Evolution of the yearly number of publications dedicated to biological control of plant 

diseases based on a survey of the CAB Abstracts ® database. 

This survey was further refined by entering keywords describing some of the major plant 

pathogens/diseases of cultivated crops in Europe, alone or cross-referenced with keywords 

indicating biocontrol. Among studies published in the period between 1973 and 2008 on these 

plant pathogens and pests, the percentage dedicated to biological control was substantial, but 

unequally distributed (Table 1). It was notably higher for studies on soil-borne (9.5% ± 1.6% as 

average ± standard error) than for those on air-borne diseases (2.8% ± 0.7%). 

1

Nicot et al. 

Table 1: Scientific papers published between 1973 and 2008 on biological control against major 

plant diseases (from CAB Abstracts ® database). 

Disease or plant pathogen 

Total number 

of references 

References on biological control 

% 

Soil-borne: 

Fusarium 34 818 1 925 5.5 

Rhizoctonia 10 744 1 278 11.9 

Verticillium 7 585 592 7.8 

Pythium 5 772 821 14.2 

Sclerotinia 5 545 456 8.2 

Air-borne: 

rusts 29 505 360 1.2 

powdery mildews 18 026 251 1.4 

Alternaria 12 766 415 3.3 

anthracnose 12 390 351 2.8 

Botrytis 9 295 705 7.5 

downy mildews 8 456 80 1.0 

Phytophthora infestans 5 303 61 1.1 

Monilia rot 1 861 81 4.3 

Venturia 3 870 104 2.7 

Inventory of potential biocontrol agents (microbials, botanicals, other natural 

compounds) 

The scientific literature described above was further examined to identify biocontrol compounds 

and microbial species reported to have a successful effect. Due to the great abundance of 

references, it was not possible to examine the complete body of literature. The study was thus 

focused on several key diseases selected for their general importance on cultivated crops, and in 

particular on those crops studied in the case studies of the European Network for Durable 

Exploitation of crop protection strategies (ENDURE * ). 

Methodology 

Three steps were followed. The first step consisted in collecting the appropriate literature references 

for the selected key diseases/plant pathogens to be targeted by the study. The references were 

extracted from the CAB Abstracts ® database and downloaded to separate files using version X1 of 

EndNote (one file for each target group). The files were then distributed among the contributors of 

this task for detailed analysis. 

In the second step, every reference was examined and we recorded for each: 

- the types of biocontrol agents (Microbial, Botanical or Other compounds) under study and their 

Latin name (for living organisms and plant extracts) or chemical name 

- the Latin name of the specifically targeted pathogens, 

- the crop species (unless tests were carried out exclusively in vitro), 

- the outcome of efficacy tests. 

Two types of efficacy tests were distinguished: Controlled environment tests (including tests on 

plants and in vitro tests), and field trials. The outcome of a test was rated (+) if significant effect 

was reported, (0) if no significant efficacy was shown and (-) if the biocontrol agent stimulated 

disease development. 

* 

EU FR6 project 031499, funded in part by the European Commission 

2

Chapter 1 

To allow for the analysis of a large number of references, the abstracts were examined for the 

presence of the relevant data. The complete publications were acquired and examined only when 

the abstracts were not sufficiently precise. 

The data were collected in separate tables for each type of key target pest. For each table, they 

were sorted (in decreasing order of priority) according to the type and name of the biocontrol 

agents, the specifically targeted pest, and the outcome of efficacy tests. 

In the third step, synthetic summary tables were constructed to quantify the number of different 

biocontrol compounds and microbial species and strains reported to have successful effect against 

each type of key pathogen/disease or pest target. 

Results 

A total number of 1791 references were examined for key airborne diseases including powdery 

mildews, rusts, downy mildews (+ late blight of Potato/Tomato) and Botrytis and Monilia rots, 

together with soilborne diseases caused by Fusarium oxysporum (Table 2). Based on the 

examination of these references, successful effect in controlled conditions was achieved for all 

targets under study with a variety of species and compounds (Appendices 1 to 6, Table 3). 

Table 2: 

Numbers of references on biocontrol examined per group of disease/plant pathogen. 

Target disease / plant 

pathogen 

Botrytis 

Relevance to 

ENDURE Case 

Studies 

OR, FV, GR* 

(postharvest) 

Number of 

references 

examined 

Period of 

publication 

examined 

880 1998-2008 

Powdery mildews all 166 1998-2008 

Rusts AC, FV, OR 154 1973-2008 

Downy mildews + 

Phytophthora infestans 

FV, GR, PO, TO 349 1973-2008 

Monilinia rot OR 194 1973-2008 

Fusarium oxysporum FV, TO 48 2007-2009 

*AC: Arable Crops; FV: Field Vegetables; GR: Grapes; OR: orchard; PO: Potato; TO: Tomato 

Concerning airborne diseases and pathogens, the largest number of reported successes was 

achieved with microbials, but there is a growing body of literature on plant and microbial extracts, 

as well as other types of substances (Table 3). On average, reports of success were far more 

numerous for experiments in controlled conditions (in vitro or in planta) than for field trials. 

Very contrasted situations were also observed depending on the type of target 

disease/pathogen, with rare reports on the biocontrol of rusts and mildews compared to Botrytis, 

despite the fact that the literature was examined over a 35 year period for the former diseases and 

only over the last 10 years for the latter. 

In total in this review, 157 species of micro-organisms have been reported for significant 

biocontrol activity. They belong to 36 genera of fungi or oomycetes, 13 of yeasts and 25 of 

bacteria. Among them, 29 species of fungi/oomycetes and 18 bacteria were reported as successful in 

the field against at least one of the five key airborne diseases included in this review (Table 4). 

3

Nicot et al. 

Table 3: Numbers of different biocontrol compounds and microbial species reported as having 

successful effect against key airborne pathogens/diseases of selected crops. Detailed 

information and associated bibliographic references are presented in Appendices 1 to 5 

Botanicals Microbials y Others z 

Target plant pathogen / 

laboratory 

laboratory 

laboratory 

disease 

tests x field trials 



Botrytis 

in vitro 26 - 31 b, 21 f - 7 - 

legumes 4 2 10 b, 12 f 3b, 9 f 0 0 

protected vegetables 0 1 22 b, 24 f 8 b, 9 f 5 1 

strawberry 0 0 14 b, 21 f 2 b, 13 f 7 1 

field vegetables 0 0 5 b, 15 f 2 f 0 0 

grapes 1 3 5 b, 27 f 5 b, 13 f 0 1 

pome/stone fruits 1 0 12 b, 35 f 2 b, 6 f 4 0 

others 3 0 15 b, 25 f 6 b, 6 f 0 0 

Powdery mildews 

Grape 1 1 4b; 10f 2b; 12f 3 2 

Arable crops 1 0 2b;9f 1b 5 0 

Strawberry 0 0 4b; 6f 0 0 0 

Cucurbitaceae 4 0 14b; 22f 4b; 9f 9 1 

Pome/stone fruits 0 0 3f 1f 0 0 

Pepper 1 0 4f 0 1 0 

Tomato 5 0 4b; 5f 1f; 1b 0 0 

Various 2 0 2b; 10f 1b; 1f 5 0 

Rusts 

arable crops 0 0 5 b, 6 f 2 b 2 0 

others 0 0 8 b, 13 f 0 1 0 

Downy mildews + late 

blight 

grapes 2 4 2 f 3 b, 2 f 2 3 

field vegetables 0 0 4 0 4 6 

potato 9 1 8 b, 10 f 5 b, 4 f 3 1 

tomato 2 1 5 b, 5 f 4 b 12 1 

Monilia rot 

in vitro 0 - 8 - 1 - 

pome fruit 0 0 7 0 0 0 

stone fruit 0 1 23b, 19 7b, 7f 2 2 

others 0 0 1b 2b, 1f 0 0 

x tests conducted in vitro and/or in planta in controlled conditions 

y b: bacteria; f: fungi / oomycetes / yeasts 

z including culture filtrates and extracts from microorganisms 

4

Chapter 1 

Table 4: 

Microbial species of fungi/oomycetes, yeasts and bacteria reported to have a significant 

effect against five main types of airborne diseases or pathogens in laboratory conditions 

or in the field (yellow highlight). Bibliographic references are presented in Appendices 1 

to 5. 

A. Fungi and oomycetes 

Target disease / pathogen 

Microbial species 

Powdery 

Botrytis 

mildew 

Rust 

Acremonium spp. 

others 

cereals, 

Acremonium alternatum 

protected 

vegetables 

A. cephalosporium grapes 

A. obclavatum others 

Alternaria spp. grapes cereals 

Downy mildew, 

late blight 

A. alternata others grapes 

fruits, grapes, 

strawberry, 

Ampelomyces quisqualis 

protected 

vegetables, 

others, 

Aspergillus spp. others tomato 

A. flavus others 

Beauveria sp 

protected vegetables 

Botrytis cinerea nonaggressive 

strains 

legumes 

Chaetomium cochlioides 

grapes 

C. globosum legumes 

Cladosporium spp. flowers others 

C. chlorocephalum others 

C. cladosporioides flowers, legumes others 

C. oxysporum flowers others others 

C. tenuissimum strawberry 

field vegetables, 

others 

Monillia rot 

flowers, legumes, 

Clonostachys rosea 

others, strawberries, 


protected vegetables, 

Coniothyrium spp. 

grapes 

C. minitans field vegetables 

Cylindrocladium 

others 

Drechslera hawaiinensis 

others 

Epicoccum sp 

flowers, grapes, field 

vegetables 

E. nigrum legumes, strawberries plum, peach 

E. purpurascens apple, cherry 

Filobasidium floriforme 

fruits 

Fusarium spp. flowers others 

F. acuminatum cereals 

F. chlamydosporum others 

F. oxysporum cereals tomato 

F. proliferatum grapes 

Galactomyces geotrichum 

fruits 

5

Nicot et al. 

Table 4 (continued) 

Gliocladium spp. 

grapes, protected 

vegetables, others 

G. catenulatum 


legumes 

G. roseum 

flowers, grapes, 

legumes, others 

others 

blueberry 

G. virens 

strawberries, field 

vegetables 

potato, others 

G. viride protected vegetables 

Lecanicillium spp. 

protected 

vegetables 

L. longisporum 

protected 

vegetables 

Meira geulakonigii 

protected 

vegetables 

Microdochium dimerum 



Microsphaeropsis ochracea field vegetables 

Muscodor albus fruits, grapes peach 

Paecilomyces farinosus 

cereals 

P. fumorosoroseus 

protected 

vegetables 

Penicillium spp. fruits, field vegetables others potato, tomato 

P. aurantiogriseum legumes potato 

P. brevicompactum legumes 

P. frequentans plum, peach 

P. griseofulvum 

legumes, field 

vegetables 

P. purpurogenum peach 

P. viridicatum potato 

Phytophthora cryptogea 

potato 

grapes, 

Pseudozyma floculosa 

protected 

vegetables, 

Pythium oligandrum protected vegetables 

P. paroecandrum grapes 

P. periplocum grapes 

Rhizoctonia flowers potato 

Scytalidium 

grapes 

S. uredinicola others 

Sordaria fimicola 

apple 

Tilletiopsis spp. 

grapes 

T. minor others 

Trichoderma spp. 


legumes, strawberries, 


potato 

others 

T. asperellum strawberries 

T. atroviride legumes, strawberries peach 

T. hamatum flowers, legumes 

T. harzianum 


others, 

grapes, potato, 

legumes, strawberries, 

strawberry, 

tomato, field 


others 

protected 

vegetables, 


vegetables, 

others 

others 

cherry, peach 

T. inhamatum flowers 

T. koningii 


vegetables 

peach 

T. lignorum others 

6

Chapter 1 


T. longibrachiatum strawberries 

T. polysporum strawberries apple 

T. taxi protected vegetables 

T. virens grapes 

T. viride 

fruits, grapes, legumes, 

strawberries, field others others potato, others peach 


Trichothecium 

grapes 

T. roseum grapes, legumes 

Ulocladium sp. 

grapes, field vegetables 

U. atrum 



vegetables, protected 

vegetables 

U. oudemansii grapes 

Ustilago maydis 


Verticillium grapes legumes 

V. chlamydosporium cereals 

V. lecanii strawberries 

cereals, 

protected 

vegetables, 

others 

legumes, others 

B. Yeasts 


Botrytis 

Powdery 

mildew 

7 


Rust 

Downy mildew, 

late blight 

Monillia rot 


apple, cherry 

Aureobasidium pullulans strawberries, protected 

vegetables 

Candida spp. tomato peach 

C. butyri fruits 

C. famata fruits 

C. fructus strawberries 

C. glabrata strawberries 

C. guilliermondii 


cherry 

vegetables 

C. melibiosica fruits 


C. oleophila 

strawberries, protected 

vegetables 

C. parapsilosis fruits 

C. pelliculosa protected vegetables 

C. pulcherrima fruits, strawberries 

C. reukaufii strawberries 

C. saitoana fruits 

C. sake fruits 

C. tenuis fruits 

Cryptococcus albidus 

fruits, strawberries, 


C. humicola fruits 

C. infirmo-miniatus fruits cherry 

C. laurentii 


cherry, peach 


Debaryomyces hansenii fruits, grapes cherry, peach 

Hanseniaspora uvarum grapes 

Kloeckera spp 

grapes 

K. apiculata fruits cherry, peach 

Metschnikowia fructicola 


strawberries 

M. pulcherrima fruits apple, apricot 

Pichia anomala 

grapes, fruits

Nicot et al. 


P. guilermondii 



P. membranaefaciens grapes peach 

P. onychis field vegetables 

P. stipitis fruits 

Rhodosporidium diobovatum protected vegetables 

R. toruloides fruits 

Rhodotorula 

peach 

flowers, fruits, 

R. glutinis 

strawberries, protected field vegetables, 

vegetables 

R. graminis flowers 

R. mucilaginosa flowers 

R. rubra protected vegetables 

Saccharomyces cerevisiae fruits 

protected 

vegetables 

Sporobolomyces roseus fruits 

Trichosporon sp. 

fruits 

T. pullulans 

fruits, grapes, protected 

vegetables 

C. Bacteria 


Acinetobacter lwoffii 

Azotobacter 

Bacillus spp. 

B. amyloliquefaciens 

Botrytis 

grapes 

grapes, strawberry, 


others 

arable crops, flowers, 

fruits, field vegetables, 

Powdery 

mildew 

protected 

vegetables 


Rust 

others 

Downy 

mildew, late 

blight 

other 

potato, field 

vegetables 


B. cereus flowers, legumes others tomato 

B. circulans protected vegetables 

B. lentimorbus others 

B. licheniformis 

fruits, strawberry, 


B. macerans legumes 

B. marismortui strawberry 

B. megaterium legumes, others 

B. pumilus fruits, strawberry tomato, others 

B. subtilis 

flowers, fruits, grapes, 

legumes, strawberry, 



B. thuringiensis strawberry 

Bakflor (consortium of 

valuable bacterial 


physiological groups) 

Brevibacillus brevis 



cereals, 

grapes, 

strawberry, 

protected 

vegetables, 

others 

grapes, 

protected 

vegetables 

legumes 


others 

grapes 

Monillia rot 

apricot 

peach 

apricot, 

blueberry, 

cherry, peach 

Burkholderia spp. 

tomato 

B. cepacia protected vegetables cherry 

B. gladii apricot 

B. gladioli flowers 

Cedecea dravisae 

others 

Cellulomonas flavigena 

tomato 

8

Chapter 1 


Cupriavidus campinensis 

Enterobacter cloacae 



Enterobacteriaceae 

strawberry 

Erwinia 

fruits, others 

Halomonas sp. 

strawberry, protected 

vegetables 

H. subglaciescola protected vegetables 

Marinococcus halophilus protected vegetables 

Salinococcus roseus 


Halovibrio variabilis protected vegetables 

Halobacillus halophilus protected vegetables 

H. litoralis protected vegetables 

H. trueperi protected vegetables 

Micromonospora coerulea protected vegetables 

Paenibacillus polymyxa 

strawberry, protected 

vegetables 

Pantoea spp. 


vegetables 

P. agglomerans 


legumes, strawberry 

protected 

vegetables 

9 

legumes 

potato 

apple, apricot, 

blueberry, 

cherry, peach, 

plum 

Pseudomonas spp. 

flowers, fruits, grapes, 

potato, tomato, 

others 

field vegetables 

field vegetables 

apricot 

P. aeruginosa protected vegetables 

P. aureofasciens cereals cherry 

P. cepacia strawberry peach 

P. chlororaphis strawberry cherry 

P. corrugata peach 

P. fluorescens 

P. putida 


legumes, strawberry, 


others 

flowers, legumes, 


others 

cereals, , 

protected 

vegetables 

others 

P. syringae 

fruits, strawberry, field 

vegetables 

grapes 

P. reactans strawberry 

P. viridiflava fruits 

Rhanella spp. 

R aquatilis 

fruits 

Serratia spp. 

S. marcescens flowers 

S. plymuthica protected vegetables 

Stenotrophomonas 

maltophilia 

Streptomyces spp. 

S. albaduncus legumes 

S. ahygroscopicus protected vegetables 

S. exfoliatus legumes 

S. griseoplanus legumes 

S. griseoviridis 


others 

S. lydicus protected vegetables 

S. violaceus legumes 

Virgibacillus marismortui strawberry 

Xenorhabdus bovienii 

X. nematophilus 

protected 

vegetables 

legumes 

cereals 

legumes 


tomato, others 

potato 

potato 

tomato 

potato 

blueberry, 

cherry 

apple, peach

Nicot et al. 

One striking aspect of this inventory is that although the five target diseases / pathogens 

included in our review are airborne and affect mostly the plant canopy, the vast majority of cited 

biocontrol microorganisms are soil microorganisms. The scarcity of biocontrol agents originating 

from the phyllosphere could be due to actual lack of effectiveness, or it could be the result of a bias 

by research groups in favour of soil microbes when they gather candidate microorganisms to be 

screened for biocontrol activity. This question would merit further analysis as it may help to devise 

improved screening strategies. As "negative" results (the lack of effectiveness of tested 

microorganisms, for example) are seldom published, the completion of such an analysis would in 

turn necessitate direct information from research groups who have been implicated in screening for 

biocontrol agents, or the development of a specific screening experiment comparing equal numbers 

of phyllosphere and of soil microbial candidates. 

Another striking aspect is that most of the beneficial micro-organisms inventoried in this study 

(49 fungi/oomycetes, 28 yeasts and 41 bacteria) are cited only for biocontrol of one of the five types 

of airborne diseases included in the survey (Figure 2). However, several species clearly stand out 

with a wide range of effectiveness, as they were successfully used against all five types of target 

diseases on a variety of crops. This includes the fungi Trichoderma harzianum and Trichoderma 

viride (2 of 12 species of Trichoderma reported as biocontrol-effective in the reviewed literature) 

and the bacteria Bacillus subtilis and Pseudomonas fluorescens. 

Number of species 

50 

45 

40 

35 

30 

25 

20 

15 

10 

5 

0 

fungi / oomycetes 

yeasts 

bacteria 

1 2 3 4 5 

Number of controlled target diseases / pathogens 

Figure 2: 

Range of efficacy of 157 microbial biocontrol agents against five main types of airborne 

diseases. Detailed data are presented in Table 4. 

Concerning Fusarium oxysporum. A data base interrogation with the key words “Fusarium 

oxysporum AND biological control” provided 2266 for the period 1973-2009. Using these key 

words we did not select only papers regarding biological control of diseases induced by F. 

oxysporum but also all the paper dealing with the use of strains of F. oxysporum to control diseases 

and weeds. There are quite many papers dealing with the use of different strains of F. oxysporum to 

control Broom rape (orobanche) and also the use of F. oxysporum f. sp. erythroxyli to eradicate 

coca crops. 

We decided to limit our review to the two last years and to concentrate on references for which 

full text was available on line. Finally we reviewed 48 papers. All these papers were dealing with 

the selection and development of micro-biological control agents; only two were considering others 

methods. One was addressing the use of chemical elicitors to induce resistance in the plant; the 

10

Chapter 1 

other was aiming at identifying the beneficial influence of non-host plant species either used in 

rotation or in co-culture. Based on this very limited number of papers the formae speciales of F. 

oxysporum the most frequently studied was F.o. f. sp. lycopersici (17 studies). Other included f. spp. 

melonis, ciceris, cubense, niveum and cucumerinum. The antagonists studied included Bacillus spp 

and Paenibacillus (16 papers), Trichoderma spp. (14 papers), fluorescent Pseudomonads (7 papers), 

Actinomycetes (5 papers), non pathogenic strains of F. oxysporum (5 papers), mycorrhizal fungi 

and Penicillium. 

Most of the publications (28) reported on in vitro studies. Among them a few concerned the 

mechanisms of action of the antagonists, the others just related screening studies using plate 

confrontation between the antagonists and the target pathogens. In most of these papers (22) the in 

vitro screening was followed by pot or greenhouse experiments aimed at demonstrating the capacity 

of the antagonist to reduce disease severity or disease incidence after artificial inoculation of the 

pathogen. Finally only 9 publications report results of field experiments. Most of these papers 

concluded on the promising potential of the selected strains of antagonists able to decrease disease 

incidence or severity by 60 to 90%. Generally speaking, this limited literature review showed that 

most of the lab studies are not followed by field studies. There is a need for implementation of 

biological control in the fields. 

Identified knowledge gaps 

Several types of knowledge gaps were identified in this review. They include: 

- the near absence of information on biocontrol against diseases of certain important European 

crops such as winter arable crops. 

- the scarcity of reports on biocontrol against several diseases of major economic importance on 

numerous crops, such as those caused by obligate plant pathogens (rusts, powdery mildews, 

downy mildews) 

- the still limited (but increasing) body of detailed knowledge on specific mechanisms of action 

and their genetic determinism. The little knowledge available at the molecular level is 

concentrated on few model biocontrol agents such as Trichoderma and Pseudomonas. 

- the still very limited information on secondary metabolites produced by microbial biocontrol 

agents 

- the lack of understanding for generally low field efficacy of resistance-inducing compounds 

- the lack of knowledge on variability in the susceptibility of plants pathogens to the action of 

BCAs and on possible consequences for field efficacy and its durability. 

References 

Due to their high number, the references used in this chapter are presented, together with 

summary tables, in Appendices 1 to 6. 

11

Chapter 2 


2. Beneficials for augmentative biocontrol against insect pests. 

The grapevine case study 

Massimo Giorgini 

CNR, Istituto per la Protezione delle Piante, via Università 133, 80055 Portici (NA), Italy 

Bibliographic survey on augmentative biological control against arthropod pests in 

selected crops 

We carried out a preliminary bibliographic survey to quantify the literature on augmentative 

biological control of pests published from 1973 to 2008. The survey was restricted to crops relevant 

to case studies of ENDURE. They included grapevine; orchards: apple and pear; arable crops: corn 

and wheat; field vegetables: carrot and onion. Augmentative biological control (Van Driesche & 

Bellows, 1996) comprises of inoculative augmentation (control being provided by the offspring of 

released organisms) and inundative augmentation (control expected to be performed by the 

organisms released, with little or no contribution by their offspring). 

Our bibliographic survey was conducted by using the CAB Abstracts database by entering the 

name of each crop and one key word selected from the following list in order to retrieve the 

maximum number of references. For each selected crop, the key words used for the bibliographic 

survey were: a) augmentative biological control; b) augmentation biological control; c) inoculative 

biological control; d) inundative biological control. The survey with these key words produced a 

very low number of results all of which were examined. For this reason we added two key words 

that were more general: e) insects biological control; f) mites biological control. For the searching 

criteria a to d, total records will be examined. In this case, given the extremely high number of 

records, only references within the period 1998-2008 were examined to select only the publications 

concerning the augmentative biological control. The results of this survey are reported in Appendix 

7. 

The analytical review of the scientific literature on augmentative biological control, presented 

in the rest of this chapter, was then focused on grapevine. 

Status of researches on augmentation of natural enemies to control arthropod pests in 

grapevine 

The references extracted from the CAB Abstracts database, following the criteria described in the 

previous paragraph, were examined to identify those concerning the use of natural enemies in 

augmentation biological control in grapevine. The abstracts of 607 references were examined and 

only 70 papers reported data on application and efficiency of augmentative biocontrol (Table 5). 

12

Chapter 2 

Table 5: 

References extracted from the CAB Abstracts database and examined for reviewing 

augmentation biological control in grapevine. 

Key words 

Total records 1998-2008 

(1973-2008) 

Augmentative biological control 7 6 

Augmentation biological control 10 6 

Inoculative biological control 4 1 

Inundative biological control 7 3 

Insects biological control 373 

Mites biological control 190 

Total references examined 28 579 

Total references showing data on 

70 

augmentative biocontrol 

The survey includes records for grapevine, grape and vineyard. 

Results 

Very few papers (62) on augmentative biocontrol in grapevine have been published during the period 1998-2008, with 

an average of 5.6 publications per year. Most references (93.5%) showed data on biological control of insects and only 

4 papers on the biological control of mites were published (Figure 3). 

Figure 3: 

Number of papers per year published during 1998-2008 concerning augmentative 

biological control of pests in grapevine. 

12 

10 

8 

6 

4 

2 

0 

1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 

biocontrol of insect pests 

biocontrol of mite pests 

The data extracted from the abstracts of the selected references were collected analytically in 

separate tables for each group of biocontrol agents (Appendix 8) and references were sorted 

chronologically (starting from the eldest). For each species of biocontrol agent, target species of 

pest, Country, type of augmentation (inundative, inoculative), type of test (laboratory, field), 

efficacy of biocontrol, additional information and results were reported. 

13

Giorgini 

Data reported in Appendix 8 were summarized in Table 6, Table 7, Table 8, Figure 4 and 

Figure 5. A list of the biocontrol agents used in augmentative biological control in grapevine is 

reported in Table 6 and Figure 4. A list of groups and species of the targeted pests and the 

antagonists used for their control is reported in Table 7 and Figure 5; the efficacy of biocontrol 

agents is reported in Table 8. 

The group of pests on which the highest number of researches on augmentative biocontrol has 

been carried out is Lepidoptera (60% of total references) with the family Tortricidae representing 

the main target (55%) (Figure 5) including the grape berry moths key pests Lobesia botrana and 

Eupecilia ambiguella (Table 7). Bacillus thuringiensis has resulted the most frequently used 

biocontrol agent against Lepidoptera by achieving an effective control of different targets in 

different geographic areas (Table 7, Table 8, Appendix 8.7). We sorted 28 references (39% of the 

total citations) dealing with the use of B. thuringiensis of which 23 references were referred to the 

control of L. botrana. The augmentation of egg parasitoids of the genus Trichogramma 

(Hymenoptera: Trichogrammatidae) resulted the alternative strategy to B. thuringiensis to control 

Lepidoptera Tortricidae (13 references, 16% of total citations) (Table 7, Table 8). Field evaluations 

indicated T. evanescens as a promising biocontrol agent of L. botrana (El-Wakeil et al., 2008 in 

Appendix 8.1). 

Fewer researches were carried out on augmentative biocontrol of other group of pests. First in 

the list were mealybugs (Hemiptera: Pseudococcidae) (9 references, 13% of the total citations). In 

field evaluations (4 papers) parasitoid wasps of the family Encyrtidae have resulted extremely 

active and promising to be used in augmentative biocontrol of mealybugs (Appendix 8.2). 

Antagonists used in augmentative biocontrol in grapevine were mainly represented by insect 

pathogens (59% of the total citations), including the bacterium B. thuringiensis, fungi and 

nematodes (Figure 4, Table 6). Beside the efficacy of B. thuringiensis, promising results were 

obtained from researches in the control of the grape phylloxera Daktulosphaira vitifolie, a gallforming 

aphid, by soil treatments with the fungus Metarhizium anisopliae (Table 8, Appendix 8.5). 

Once controlled by grafting European grape cultivars onto resistant rootstocks, the grape phylloxera 

has gone to resurgence in commercial vineyards worldwide and new biological control strategy 

could be necessary to complement the use of resistant rootstocks and to avoid the distribution of 

chemical insecticides in the soil. 

Entomophagous arthropods, including parasitoid wasps and predators represented 41% of the 

total citations (Figure 4, Table 6). Best results were obtained from researches on parasitoids (18 

references), namely the use of Trichogrammatidae and Encyrtidae in augmentative biocontrol of 

grape moths (Tortricidae) and mealybugs (Pseudococcidae) respectively (Table 7, Table 8, 

Appendix 8.1 and 8.2). Among predators, augmentation of Phytoseiidae mites has produced some 

positive results in controlling spider mites and eriophyid mites on grape (Table 7, Table 8, 

Appendix 8.3). 

Brief considerations 

Key pests of grapevine like L. botrana and E. ambiguella can be controlled effectively with 

augmentative strategies that rely on the use of B. thuringiensis. To date, formulations of B. 

thuringiensis are currently used in IPM strategies. The specificity of B. thuringiensis could be a 

problem in those vineyards where other pests can reach the status of economically importance, if 

not controlled by indigenous and/or introduced natural enemies. Researches on augmentative 

biocontrol should be implemented in order to develop new strategies to solve problems related to 

emerging pests and alternatives to B. thuringiensis if resistant strains should appear in target 

species. 

References 

Due to their high number, the references for this chapter are presented in Appendix 8. 

14

Chapter 2 

Table 6: 

Biocontrol agents evaluated in researches on augmentative biological control of pests in 

grapevine. 

Target pests and biocontrol agents 

References 

before 1998 

References 

1998-2008 

Number of 

citations 

BIOLOGICAL CONTROL OF INSECTS 

Bacteria 

[1 species: 2 subspecies] 

0 28 

- Bacillus thuringiensis 

28 

(subsp. kurstaki, subsp. aizawai) 

Fungi [5 species] 0 10 

- Metarhizium anisopliae 7 

- Beauveria bassiana 2 

- Beauveria brongniartii 1 

- Verticillium lecanii 1 

- Clerodendron inerme 1 

Nematodes [5 species] 1 3 

- Steinernema spp. 2 spp. 2 

- Heterorabditis spp. 3 spp. 3 

Parasitoid Hymenoptera [15 species] 2 16 

- Trichogramma spp. (Trichogrammatidae) 10 spp 13 

- Coccidoxenoides spp. (Encyrtidae) 2 spp. 2 

- Anagyrus spp. (Encyrtidae) 2 spp. 3 

- Muscidifurax raptor (Pteromalidae) 1 spp. 1 

Predators [5 species] 2 4 

- Chrysoperla (Neuroptera: Chrysopidae) 3 spp. 3 

- Cryptolaemus montrouzieri 

2 

(Coleoptera: Coccinellidae) 

- Nephus includens (Coleoptera: Coccinellidae) 1 

BIOLOGICAL CONTROL OF MITES 

Predators (Acari: Phytoseiidae) [4 species] 

2 4 

- Typhlodromus pyri 5 

- Kampimodromus aberrans 2 

- Amblyseius andersoni 1 

- Phytoseiulus persimilis 1 

15

Giorgini 

Table 7: 

Number of references on augmentative biocontrol agents per group and species of target pest in grapevine. 

Pest References Bacillus 

thuringiensis 

(2 subspecies) 

Trichogramma 

(10 species) 

other 

parasitoids 

(5 species) 

Predators of 

mites 

Acari: 

Phytoseidae 

(4 species) 

Predators of 

insects 

Coleoptera: 

Coccinellidae 

(2 species) 

Predators of 

insects 

Neuroptera: 

Chrysopidae 

(3 species) 

Fungi 

(5 species) 

Nematodes 

(5 species) 

Lepidoptera: 

39 

Tortricidae 

Lobesia botrana 

28 23 5 

(grape berry moth) 

Eupoecilia ambiguella 

6 3 3 


Epiphyas postvittana 

3 3 

(light brown apple moth) 

Argyrotaenia sphaleropa 3 1 2 

(South American tortricid moth) 

Bonagota cranaodes 

2 2 

(Brasilian apple leafroller) 

Endopiza viteana 

2 2 


Sparganothis pilleriana 1 1 

(grape leafroller) 

Epichoristodes acerbella 1 1 

(South African carnation tortrix) 

Lepidoptera: 

1 

Pyralidae 

Cryptoblabes gnidiella 

1 1 

(honey moth) 

Lepidoptera: 

1 

Arctiidae 

Hyphantria cunea 

1 

(fall webworm) 

Lepidoptera: 

2 

Sesiidae 

Vitacea polistiformis 2 2 

16


Chapter 2 

Hemiptera: 

9 

Pseudococcidae 

Planococcus ficus 6 4 

2 

Encyrtidae 

Pseudococcus maritimus 1 1 

Pseudococcus longispinus 1 

Maconellicoccus hirsutus 1 

1 

Encyrtidae 

Hemiptera: 

3 

Cicadellidae 

Erythroneura variabilis 3 3 

Erythroneura elegantula 3 3 

Hemiptera: 

5 

Phylloxeridae 

Daktulosphaira vitifoliae 

4 1 

(grape phylloxera) 

Diptera: 

1 

Tephritidae 

Ceratitis capitata 1 1 

Pteromalidae 

Coleoptera: 

2 

Scarabeidae 

Melolontha melolontha 2 1 1 

Thysanoptera: 

3 

Thripidae 

Frankliniella occidentalis 2 2 

grape thrips 1 1 

Acari: 

6 

Tetranichidae 

Panonychus ulmi 5 5 

Tetranychus urticae 1 1 

Tetranychus kanzawai 1 1 

Eotetranychus carpini 2 2 

Acari: 

2 

Eriophyidae 

Calepitrimerus vitis 1 1 

Calomerus vitis 1 1 

17

Giorgini 

Table 8: 

Number of references reporting data on the efficacy of augmentative biocontrol of 

pests in grapevine. 

Groups of Pests Biocontrol agents Total 

number of 

references 

Number of references reporting data 

on efficacy in pest and related 

damage control * 

Laboratory assays Field evaluation 

Lepidoptera: 

Tortricidae 

Lepidoptera: 

Pyralidae 

Lepidoptera: 

Arctiidae 

Lepidoptera: 

Sesiidae 

Hemiptera: 


Hemiptera: 

Cicadellidae 

Hemiptera: 

Phylloxeridae 

Diptera: 

Tephritidae 

Acari: 

Tetranichidae 

Acari: 

Eriophyidae 

Coleoptera: 

Scarabeidae 

Thysanoptera: 

Thripidae 

Bacillus thuringiensis 26 2 + 16 + 

1 - 

Trichogramma spp. 

parasitoids 

13 

1 - 

9 + 

1 - 

Bacillus thuringiensis 1 1 + 

Bacillus thuringiensis 1 1 + 

Nematodes 2 2 + 1 + 

1 + (greenhouse) 

Encyrtidae parasitoids 5 4 + 

Coccinellidae 3 1 + (greenhouse) 

Fungi 1 1 + 

Chrysopidae 3 2 - 

Nematodes 1 1 + 

Fungi 5 1 + 2 + 

1 - 

Pteromalidae parasitoids 1 1 + 1 + 

Phytoseidae 6 4 + 

Phytoseidae 2 1 + 

Nematodes 1 1 + 

Fungi 1 1 + 

Fungi 3 1 + 2 + 

* + means effective, - means not effective biocontrol agent 

18

Chapter 2 

Bacillus thuringiensis: 28 (39%) 

Fungi: 10 (14%) 

Nematodes: 4 (6%) 

Parasitoid Hymenoptera: 18 (25%) 

Predators of insects (Chrysopidae, 

Coccinellidae): 6 (8%) 

Predators of mites (Phytoseidae): 6 (8%) 

Figure 4: 

Groups of biocontrol agents investigated in augmentative biological control 

researches in grapevine. Number of references for each group is reported. 

Lepidoptera Tortricidae: 39 (55%) 

Lepidoptera Sesiidae: 2 (3%) 

Lepidoptera Arctiidae: 1 (1%) 

Lepidoptera Pyralidae: 1 (1%) 

Hemiptera Pseudococcidae: 9 (13%) 

Hemiptera Phylloxeridae: 5 (7%) 

Hemiptera Cicadellidae: 3 (4%) 

Acari Tetranichidae and Eriophyidae: 6 (8%) 

Thysanoptera Thripidae: 3 (4%) 

Coleoptera Scarabeidae: 2 (3%) 

Diptera Tephritidae: 1 (1%) 

Figure 5: 

Groups of target pests investigated in augmentative biological control researches 

in grapevine. Number of references for each group is reported. 

19

Chapter 3 

Potential of biocontrol based on published research. 

3. Research and Development in classical biological control with 

emphasis on the recent introduction of insect parasitoids 

Nicolas Ris and Jean Claude Malausa 

INRA, UE 1254, Unité expérimentale de Lutte Biologique, Centre de recherche PACA, 

400 route des Chappes, BP 167, F-06903 Sophia Antipolis, France 

Scope of the review 

Defined as “the intentional introduction of an exotic, usually co-evolved, biological control 

agent [hereafter BCA] for permanent establishment and long-term pest control’, classical 

biological control [hereafter ClBC] is a pest control strategy that has crystallized numerous 

studies since more than one century and provided numerous efficient solutions for pest 

control. The main advantages and risks of this strategy can be summarized as follows. In a 

context of the globalisation of international trade and human mobility, an ever growing 

number of exotic pests emerge locally. Such species can rapidly pullulate and jeopardize 

cultural practices. This general trend can also be favoured by global climatic changes that 

may allow the development of agronomic pests beyond their initial distribution area and 

increase their demography. Within this context, ClBC appears often to be the first way to try 

to regulate such pest populations. Moreover, when successful, ClBC appears to be very 

economic insofar as financial costs are only associated with the identification, evaluation and 

initial releases of exotic BCA. Contrary to other pest control strategy, the implication of 

practitioners and other costs are not necessary after the establishment of the BCA. The 

overall financial costs of such operations are consequently rather limited with regard to the 

durability of the pest control, in particular when the local introduction of a new BCA benefits 

from the previous experiences in other countries. Nevertheless, at least two kinds of risks are 

usually associated with ClBC. First of all, the average success rate of ClBC varies between 

10 and 30% according to the authors for a total of more than 5000 introductions worldwide 

during the last century. As consequence, such operations may also appear too risky to be 

funded. Another risk is those associated with the non-target effects. Although few cases have 

been reported, their echoes may have contributed to a more harmonized approach and in 

some countries to more or less stringent regulations. 

As consequences, classical biological programmes are at the crossroad of several 

concerns: 

- agronomic; insofar as each introduction of exotic BCA is obviously an hope for the 

producers ; 

- scientific; ClBC namely questions both ecologist and evolutionist in order to optimize the 

probability of establishment while minimizing the non-target effects. Their implication on 

such issues nevertheless depends on their own interest (in term of scientific question 

and/or possibility or publishing); 

- political; since the introduction of BCA may depend on regulation or homologation 

decided at national or international levels; 

20

Chapter 3 

- financial; since the development of ClBC is relying on various sources of funding 

(agronomic partners, scientific partners, politic institutions) with various interests and 

rationale (more or less short-term results, scientific excellence versus applied objectives). 

Within this context, global evaluations of ClBC programmes are necessary to better 

understand the evolution of this practice and try to improve its use and efficiency. This has 

been repeatedly achieved during the last years either through reviews or meta-analysis. Based 

on a large (but probably not exhaustive) bibliographic survey, the present work aims to give a 

complementary point of view with the willingness to portray a realistic “state of the art” of 

Research and Development programmes of ClBC against arthropods. This chapter also firstly 

gives a broad temporal survey of the publication and a more precise survey of the literature 

for the decade [1999; 2008]. Biocontrol programmes against arthropods were then more 

precisely detailed with the objectives to give qualitative cues about the main pests and the 

types of related studies. Finally, a particular emphasis has been put on recent introductions of 

exotic insect parasitoids. 

Based on these data, we also address some more or less important subjective 

recommendations based on our own opinion. 

Method 

A large bibliographic survey has been conducted with the CAB abstracts. Several 

combinations of key-words were used with various successes. Too broad (e.g; cases for 

which discussion about ClBC are marginal) or unprecise (e.g. cases for which a pest is not 

precised) publications were excluded. A total of 764 publications were found using the keywords 

“classical biological control” or “classical biocontrol”. 452 papers were published 

during the period [1999-2008] but about 30% were not relevant with regard to the purpose of 

this survey and have been discarded. Using the more complex combinations [“biological 

control” AND “exotic” AND “introduction”], 329 ClBC-related publications were obtained 

but only 253 dressed precisely questions related to classical biological control. 117 were 

published during the selected temporal frame but only 81 were relevant with regard to our 

objectives. Additionally, 47 ClBC-related publications were obtained using the more keywords 

association [“biological control” AND “exotic” AND “importation”] with 17 papers 

for the last ten years. Most of this literature was dedicated to the risk or regulatory aspects 

associated with the importation of exotic BCA so that only 7 relevant publications with 

regard to our objectives. Finally, 130 publications were found using “acclimatization” AND 

“biological control” for only one relevant publication for the targeted period. A total of 358 

publications were also obtained which is probably for far from being exhaustive. For 

instance, 37 new references about BCA introductions were found in addition to the first 35 

references found with the previous key-words combinations (see Table 9). Additional 

bibliographic research were also realised for some taxa (see below) 

[Remark: Although the terms “classical biological control” or “classical biocontrol” 

may be not as explicit as others (“introduction”, “importation”), the generalization of their 

use in titles, key-words or abstracts should be nevertheless used in order to improve the 

efficiency of bibliographic survey] 

21

Ris & Malausa 

General trends 

The temporal survey shows a quite regular increase of ClBC related publications with a mean 

of about 45 hits / year for the last ten years (Figure 6). Within this period, we observe a 

relative stability between the different combinations of pests and BCA (Figure 7). The main 

part of the publications (56%) of the cases deals with the biocontrol of phytophagous 

arthropods on which we will focus here. 42% of the papers deal with the biocontrol of weed. 

In this case, BCA are for 57% of the cases phytophagous insects and for 41% fungi (data not 

shown). 

More than 70 arthropod pests were listed which cover 7 orders and approximately 40 

families. As shown in Figure 8, Hemiptera and Lepidoptera were the two main orders with a 

total of 66% of the pest species and 70% of the publications. If the citation rate / order is 

highly correlated with the number of pests / order, this trend hides a great variability at the 

infra-order level. Indeed, the citation rate highly differs with regard to the pest species with a 

median of 2 papers / pest species and a range from 1 to 13 citations. The 13 most cited pests 

are listed in Figure 9. Two main observations can be drawn from this short list. 

Firstly, this list is quite equally composed of either very specialist pests like 

Phyllocnistis citrella (on Citrus species), Mononychellus tanajoa (on cassava) or Toxoptera 

citricida (on Citrus species) or more generalist taxa like Homalodisca vitripennis, Lymantria 

dispar or Pseudococcus viburni. All of them are phytophagous pests whose damage are 

linked either to their herbivory, consumption of sap or virus transmission except the 

particular case of the fire ant Solenopsis invicta which is responsible for direct nuisance on 

farmers or indirect ecological modifications in the agrosystems. 

The second observation is that the percentage of ClBC related publications / pest is 

negatively correlated with the corresponding total number of references (including also 

studies on other pest control strategies and/or various biological topics). For instance, 22% of 

the 32 references focusing on H. vitripennis explicitly deal with classical biological control 

while this percentage falls down to only 1% to 3% for well documented species like L. 

dispar, S. invicta or D. virgifera virgifera. This may be explained by the fact that ClBC is 

mainly considered as a “pionneer” pest control strategy that are developed either soon after 

the emergence of a new invasive pest or on “non biological model” for which the 

investigations on other biological aspects are limited. 

[Remark: Although Classical Biological Control can be perceived as a “pioneer” 

pest control strategies on non “biological models”, substantial investments are required on 

several biological aspects (e.g. community ecology, population genetics)] 

Biocontrol agents used 

The biocontrol agents related to ClBC (hereafter ClBCA) against arthropod species were not 

detailed in only 12% of the papers. These are in most of the cases either prospective works 

(55%) such as faunistic inventories of natural enemies on “new” pests like Diabrotica 

virgifera virgifera or retrospective studies (35%) on advanced programmes that take into 

account several BCA (see Appendix 9.1). Among the documented cases, 76% of ClBC 

programmes were based on the use of insect parasitoids. Pathogens and nematodes on one 

side and predatory arthropods on the other side are equally represented with about 12% of the 

publications for each case. 

22

Chapter 3 

Pathogens and Nematodes as candidate for ClBCA 

The particular cases of pathogens and nematodes have been recently reviewed by Hajek and 

co-workers (62, 63 3 ). Our own survey indicates that half of the papers actually deal with 

entomopathogenic fungi. Six pest species were identified including two mites (Aceria 

guerreronis and Mononychellus tanajoa) and two insects (Aphis gossypii and Coptotermes 

formosanus). However, except for the evaluation of Neozygites species against M. tanajoa 

(14, 39, 42, 43), other attempts seem to be rather limited. With regard to the catalogue of 

Hajek et al.(62), two other cases of entomopathogen fungi were missed in our own survey. 

These are the introductions of Entomophaga maigmaiga and Metarhizium anisopliae, against 

respectively the Lymantria dispar and the Curculionidae Otiorynchus nodosus for which the 

sources of Hajek and coworkers were mainly personal communications. The rather limited 

use of entomopathogenic fungi in ClBC was also confirmed by the review of Shah and 

Pell(156). The use of viruses as biocontrol agent for ClBC against arthropod pests were only 

documented fort three cases that are the Lepidoptera species Anticarsia gemmatalis (48, 127) 

and Lymantria dispar (16) and the Coleoptera Oryctes rhinoceros (81). Microspodia as 

candidate for ClBC were reported in only two studies (25, 165). The sole case of the use of 

nematodes is the study of Hurley et al. (79) who studied the extension of the use of parasitic 

nematode Deladenus siricidicola against the woodwasp Sirex noctilio. 

Predatory arthropods as candidate for ClBCA 

The literature about predatory arthropods is dominated by four case-studies. The first one is 

the classical biocontrol of the cassava green mites M. tanajoa by Typhlodromalus aripo and, 

to a lesser extent, T. manihoti. All these studies are the extension of a very large classical 

biocontrol programme at a continental scale; two main issues were addressed during the 

recent decade that are the introduction and field evaluation of T. aripo in Mozambique and 

Malawi (125, 194) and the ecological interactions with other species (14, 124, 193) or 

plants(55). The second case-study is those of the predatory ladybird Harmonia axyridis (19, 

90, 91, 137). The main concern of these publications is nevertheless not the Research and 

Development in ClBC but rather the risks of non-intended effects and geographic spray of 

this insect that is now considered as a world-wide invasive species. Another case of the use of 

ladybird is those of Cryptolaemus montrouzieri and Scymnus coccivora which have been 

successfully used to control the hibiscus mealybug Maconellicoccus hirsutus (51, 86, 103) 

which is the extension of a worldwide use of these species. The fourth main case-study is the 

classical biocontrol programme of Prostephanus truncatus, a serious pest of stored maize 

beetle using Teretrius (formerly Teretriosa) nigrescens (73, 169, 170). The lasts reported uses 

of predatory arthropods as candidate for ClBC were those of the Coleoptera Laricobius 

nigrinus against the adelgid Adelges tsugae (197) and the phytoseid Neoseiulus baraki 

against the coconut mite A. guerreronis (119). Contrary to other cases which were the 

continuity of older programmes, these two studies are associated with new BCA inventories 

undertaken during the last ten years - see respectively (196) and(99). 

Insect parasitoids as BCA 

Related journals papers and categorization of the studies 

In total, 125 publications were used for this analysis. Only 14% were associated to 

proceedings of meetings or other supports than journals. 43 different journals were identified 

but 50% of the publications were published only by five: Biological Control (21%), 

BioControl (8%), Biocontrol Science and Technology (7%), Florida Entomologist (7%) and 

3 within this Chapter, numbers in parentheses refer to references listed in Appendix 9 

23

Ris & Malausa 

Bulletin of Entomological Research (7%). Impact Factors are respectively 1.805, 1.957, 

0.874, 0.886 and 1.415. 

The types of the works were categorized according to the simplified sequential steps in 

R&D of biological programmes: BCA Inventories BCA characterization (systematic, 

molecular tools) Pest or BCA rearing BCA biology (life history traits, thermal biology, 

behavioural ecology) Pre-release survey BCA introduction Post-release survey. 

Studies related to “non-target effects” (i.e. the direct or indirect impacts of the ClBCA on 

non-target species) as well as those related to the “biocontrol disruption” (i.e. the negative 

impacts of organisms on the ClBCA) (details in Appendix 9.3) were also categorized. As 

shown in Figure 10, most of the ClBC related publications logically deals either with BCA 

biology, BCA introductions or post-release surveys which are central steps of the ClBC 

programmes. A strong discrepancy nevertheless exists between the different types of work in 

term of scientific publication; highest Impact Factors are relied to studies linked to Nonintended 

effects, Biocontrol disruption or BCA Biology. 

[Remark: The different steps of R&D in Classical Biological Control are currently 

unequally promoted with regard to “scientific criteria”, with a clear emphasis on community 

ecology including non target effects. Such trend may be detrimental to the short-term 

development of less gratifying tasks and consequently on the whole dynamism of ClBC.] 

BCA Introductions 

As shown in Table 9, 65 introductions were recorded during the period of 1991-2006. This 

list is probably not exhaustive insofar as “cryptic introductions” may have been missed. This 

list does not also cover all the R&D in classical biocontrol programmes since some 

programmes may have been interrupted before releases. A faunistic inventory of the natural 

enemies of the North American leafhopper Scaphoideus titanus has for instance been led by 

our lab in 2000-2002 but the rearing of BCA candidates (mainly dryinids and eggparasitoids) 

were not successful. 

All these releases involve 55 different biocontrol agents (all hymenopteran except 

the Pseudacteon species used against the fire ant Solenopsis invicta) and 35 pests. 57% of 

these pests were Hemiptera, other being quite equally distributed between Lepidoptera, 

Diptera, Hymenoptera and Coleoptera. 

Most of these introductions were realized against pest found on orchards and in 

particular Citrus. Other targeted crops were mainly tropical productions, ornamental or forest. 

Most of the BCA introductions (42%) were realized in Europe or neighbouring 

countries (including Mediterranean Basin) and in North America (26%). The percentages of 

introductions in other geographical areas were: Australia-New Zealand and neighbouring 

islands (12%), South America (8%), sub-Saharan Africa (8%), Pacific Islands (3%), Asia 

(1%). 

The total number of released parasitoids and number of sites were highly variable 

ranging respectively from 456 to 660000 individuals and from 2 to 132 sites. The percentage 

of establishment was 83% and, when established, high parasitism was found in 42% of the 

cases. It is noteworthy that these values are relatively high compared to other estimates and 

we are currently unable to say if this is linked to an improvement of practices or 

methodological differences or biases. 

[Remark: With regard to natural or other human-mediated introductions of exotic 

species, species flow associated with the ClBC seems to be rather limited. Although possible 

non-intended effects cannot be excluded (their studies having to be increased), we fear that 

too drastic regulations could severely disturbed R&D programmes] 

24

Chapter 3 

[Remark: Estimating the success of ClBC is difficult because of methodological 

several biases (“cryptic introductions”, barriers linked to languages and/or publishing). 

Shared international database should be necessary for more accurate estimation as well as 

an increasing traceability.] 

[Remark: In parallel with the geographical expansion of their related pests, some 

biocontrol agents have been repeatedly released and established worldwide. Population 

genetics studies in such pest-BCA interactions should be particularly interesting to 

understand local adaptations, co-evolutionary processes and ultimately, the durability of 

Classical Biological Control.] 

25

Ris & Malausa 

70 

60 

50 

Publications in CabAbstracts 

40 

30 

20 

10 

0 

1973 

1974 

1975 

1976 

1977 

1978 

1979 

1980 

1981 

1982 

1983 

1984 

1985 

1986 

1987 

1988 

1989 

1990 

1991 

1992 

1993 

1994 

1995 

1996 

1997 

1998 

1999 

2000 

2001 

2002 

2003 

2004 

2005 

2006 

2007 

2008 

Figure 6: 

Large-scale temporal survey of the publications associated with classical 

biological control 

26

Chapter 3 

100% 

80% 

60% 

P = Phytophagous arthropod ; BCA = not documented 

P = Phytophagous arthropod ; BCA = Pathogen 

P = Phytophagous arthropod ; BCA = Predator 

40% 

P = Phytophagous arthropod ; BCA = Parasitoid 

P = Other animals 

P = Weed 

20% 

0% 

1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 

Figure 7: Relative importance of the different types of biocontrol during the temporal frame [1999-2008] 

27

Ris & Malausa 

0,5 

0,4 

Hemiptera 

Percentage of citations 

0,3 

0,2 

Lepidoptera 

0,1 Acari 

Coleoptera 

Diptera 

Hymenoptera 

Thysanoptera 

0,0 

0,0 0,1 0,2 0,3 0,4 0,5 

Percentage of pests 

Figure 8: 

Number of pest species and related citation rate by orders during the period 

[1999 ; 2008] 

28

Chapter 3 

0,25 

4 

0,20 

% dedicated to ClBC 

0,15 

0,10 

8 

6 

2 

3 

0,05 

0,00 

13 

1 

12 

9 10 

11 7 

5 

0 100 200 300 400 500 600 700 800 900 

number of publications [1999 ; 2008] 

Figure 9: Relationships between the number of publications associated to the main pests and 

the relative percentage of ClBC related studies. 

Pest species are ranked in the decreasing order in number of publications : 1 : Phyllocnistis citrella ; 2 : 

Mononychellus tanajoa ; 3 : Toxoptera citricida ; 4 : Homalodisca vitripennis ; 5 : Lymantria dispar ; 6 : 

Pseudococcus viburni ; 7 : Solenopsis invicta ; 8 : Aleurocanthus spiniferus ; 9 : Bactrocera oleae ; 10 : Chilo 

partellus ; 11 : Diabrotica virgifera virgifera ; 12 : Diatraea saccharalis ; 13 : Maconellicoccus hirsutus. 

Specialist and generalist pests are respectively indicated by white and dark diamonds. 

29

Ris & Malausa 

2,0 

1,8 

Biocontrol 

disruption 

Non-target effects 

1,6 

BCA Biology 

median IF 

1,4 

1,2 

1,0 

0,8 

0,6 

BCA 

characterization 

Pre-release survey 

Rearing 

BCA inventories 

Post-release survey 

0,4 

0,2 

BCA 

0,0 

introduction 

0,00 0,05 0,10 0,15 0,20 0,25 

Frequencies of Type of work 

Figure 10: Frequencies of papers and associated median IF related to the different categories 

of work 

30

Chapter 3 

Table 9: 

Recent introductions of parasitoids as Classical Biocontrol agents 

Targeted pest Crop BCA Name 

Introduction Introduction Individuals 

Area 

Date (sites) 

Outcome 

References 

Aleurocanthus woglumi Citrus Amitus hesperidum Trinidad 2000 

1600 Establishment 

(3) High parasitism 

(White et al., 2005) 

Aleurodicus dispersus Banana Encarsia guadeloupae Spain (Tenerife) _ _ _ (Nijhof et al., 2000) 

Lecanoideus floccissimus _ _ _ 

Encarsia haitiensis Australia 1992-1996 _ Establishment (Lambkin, 2004)* 

Aleurolobus niloticus 

Orchard 

Establishment 

Eretmocerus siphonini Egypt 1998-1999 237000 

High parasitism 

(Abd-Rabou, 2002) 

Aonidiella aurantii Citrus Aphytis lingnanensis Spain 2000 _ Establishment (Pina and Verdu, 2007)* 

Aphis gossypii Vegetable Lysiphlebus testaceipes Bulgaria _ _ Establishment (Dimitrov et al., 2008)* 

Bactrocera dorsalis 

Orchard 

Establishment 

Fopius arisanus French Polynesia 2003 


(Vargas et al., 2007)* 

Bemisia tabaci 

Arable crops 

Vegetable 

Eretmocerus hayati Egypt 2000-2002 200700 Establishment (Abd-Rabou, 2004)* 

Ceratitis capitata Orchards Diachasmimorpha krausii Israel 2002-2004 75881 Establishment (Argov and Gazit, 2008)* 

(incl. Citrus) Fopius arisanus 2002-2004 258750 ? 

Fopius ceratitivorus 2002-2004 58860 Establishment 

Psyttalia concolor (complex) 2002-2004 75881 ? 

Ceroplastes rubens 

Orchard 

(incl. Citrus) 

Anicetus beneficus Papua New Guinea 2002 

Chilo sacchariphagus Sugarcane Xanthopimpla stemmator Mozambique 2001 

2200 

(2) 

5000 

(5) 

Establishment 

? 

(Krull and Basedow, 

2005) 

(Conlong and Goebel, 

2002) 

Cinara cupressivora 

Forest 

Ornamenta 

Pauesia juniperorum Mauritius 2003-2004 1500 ?_ (Alleck et al., 2006) 

Coccus viridis 

Citrus 

_ Establishment 

Diversinervus sp. near stramineus Australia _ 

Coffee 


(Smith et al., 2004)* 

Ctenarytaina eucalypti 

Forest 

Establishment (Rodriguez and Saiz, 

Psyllaephagus pilosus Chile 2001 _ 

Ornamental 

High parasitsm 2006)* 

Diaphorina citri Citrus Diaphorencyrtus aligarhensis USA _ _ _ (Hoy, 2005) 

Tamarixia radiata USA _ _ 

_ 

Diatraea saccharalis Sugarcane Cotesia flavipes USA 2001-2002 

Forest 

Dryocosmus kuriphilus 

Torymus sinensis Italy 2005-2006 

Ornamental 

Legend : _ : data not available ; ? : long-term establishment not sure ; * : additional references 

_ 

(4) 

1100 

(14) 

Failure (White et al., 2004)* 

Establishment (Aebi et al., 2007) 

31

Ris & Malausa 

Table 9: Recent introductions of parasitoids as Classical Biocontrol agents (continued) 

Hemiberlesia pitysophila Forest Coccobius azumai China 2002 _ Establishment (Wang et al., 2004)* 

(Grandgirard et al., 

Homalodisca vitripennis Wide range Gonatocerus ashmeadi Tahiti 2005 

2007a) 

14000 Establishment 

(Grandgirard et al., 


2008) 

(Petit et al., 2008) 

Hypothenemus hampei Coffee Cephalonomia stephanoderis Cuba _ 

_ 

? 

(Murguido Morales et 

Phymastichus coffea Colombia _ 

Lilioceris lilii Ornamental Diaparsis jucunda USA _ _ _ 

(2) 

_ 

(41) 

Establishment 

al., 2008)* 

(Aristizabal et al., 

2004)* 

(Casagrande and 

Tewksbury, 2005)* 

Lemophagus errabundus _ _ _ 

Tetrastichus setifer 2001 

1700 

(Tewksbury et al., 

_ 

(21) 

2005)* 

Liriomyza trifolii Vegetables Dacnusa sibirica Egypt _ 90000 ? (Abd-Rabou, 2006)* 

Diglyphus isaea _ 90000 ? 

Listronotus bonariensis Pasture Microctonus hyperodae New Zealand 1991-1998 

66000 

(McNeill et al., 2002) 

_ 

(121) 

(Phillips et al., 2008) 

Maconellicoccus hirsutus Wide range Anagyrus kamali North America 

Metcalfa pruinosa Wide range Neodryinus typhlocybae Greece 2006 

Ophelimus maskelli 

Forest 

Ornamental 

Closterocerus chamaeleon Israel 2005-206 

Closterocerus sp. Italy _ 

Paracoccus marginatus Wide range Acerophagus papayae Palau 2003-2004 _ 

Anagyrus loecki 2003-2004 _ 

Pseudleptomastix mexicana 2003-2004 _ Failure 


_ 

_ 

12000 

(6) 

_ 

(5) 

Establishment 


Establishment 

Establishment 


Establishment 


Establishment 


Establishment 


(Kairo et al., 2000) 

(Anagnou-Veroniki et 

al., 2008) 

(Protasov et al., 2007)* 

(Rizzo et al., 2006)* 

(Muniappan et al., 2006) 

32

Chapter 3 

Table 9: Recent introductions of parasitoids as Classical Biocontrol agents (continued) 

Phyllocnistis citrella 

Citrus 

Ageniaspis citricola Morocco 1995-1996 _ Failure (Rizqi et al., 2003) 

USA _ _ 

Establishment 


(Hoy, 2005) 

Italy 1995 _ Failure (Siscaro et al., 2003) 

Italy 1996-1997 _ 

Establishment 


(Siscaro et al., 1999) 

USA 1999 

25000 

(132) 

(Paiva et al., 2000) 

Argentina 2001-2004 ? (Zaia et al., 2006) 

Brazil 1999 25000 _ (Paiva et al., 2000)* 

Cirrospilus ingenuus Morocco _ _ _ (Rizqi et al., 2003) 

Cirrospilus quadristriatus [C. 

Establishement 

USA _ _ 

ingenuus] 

(Hoy, 2005) 

Citrostichus phyllocnistoides Italy 1995 _ 

Establishment 

(Siscaro et al., 2003) 

Morocco 2000 _ Establishment (Rizqi et al., 2003) 

Spain 1996-1999 _ 

Establishment (Garcia-Mari et al., 

High parasitism 2004)* 

Quadrastichus sp Morocco _ _ (Rizqi et al., 2003) 

Italy 1995 _ Failure (Siscaro et al., 2003) 

Italy 1996-1997 _ Failure (Siscaro et al., 1999) 

Semielacher petiolatus Morocco 1996-1997 _ Establishment (Rizqi et al., 2003) 

Pseudococcus viburni Orchard Pseudaphycus maculipennis New Zealand 2001 _ _ (Charles, 2001) 

Saissetia coffeae Olive Coccophagus cowperi Egypt 2001-2003 300000 Establishment (Abd-Rabou, 2005)* 

Siphoninus phillyreae Orchard Eretmocerus siphonini Egypt 1998-1999 237000 

Establishment 


(Abd-Rabou, 2002) 

Sirex noctilio Forest Ibalia leucospoides South Africa 1998-2001 456 Establishment (Tribe and Cillie, 2004)* 

Solenopsis invicta _ Pseudacteon curvatus USA 2003 

10100 

(2) 

Establishment (Vazquez et al., 2006) 

Pseudacteon obtusus USA 2006 ? (Gilbert et al., 2008) 

Pseudacteon tricuspis USA 1999-2001 Establishment 

Tephritidae sp. 

Orchard 

34000 

Diachasmimorpha longicaudata Brazil 2002 

(incl. Citrus) 

(2) 

Failure (Alvarenga et al., 2005) 

Toxoptera citricida Citrus Lipolexis oregmae USA 2000-2002 33500 Establishment 

(Hoy, 2005) 

(Persad et al., 2007) 

Yponomeuta malinellus * Orchard Ageniaspis fuscicollis Canada 1987-1997 _ 

Establishment (Cossentine and 

Kuhlmann, 2007)* 


33

Chapter 4 

Registered Biocontrol Products and their use in Europe 

Ulf Heilig 1 , Philippe Delval 2 and Bernard Blum 1 

1 International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel, 

Switzerland 

2 ACTA, 1 avenue Claude Bourgelat, F-69680 Marcy l'Etoile, France 

Collection of information 

A small team formed by ACTA and IBMA conducted a survey on biological active substances 

approved in the European Union and on Biological Control Products (BC products) authorised in 

five European countries. The investigation focused on crops covered by ENDURE RA1case studies. 

The frame of the present survey was defined in a meeting on 9 th January 2009 in Basle, and the 

work was performed during the period from April to September 2009. 

To compile a list of registered biocontrol products, the online EU Pesticides Database was 

consulted on 21 st April 2009. Data were retrieved and the list was reorganised and the information 

about use categories complemented with the help of the inclusion directives where necessary. 

Substances deemed suitable for biocontrol were identified and it was decided to distinguish four 

major groups: micro-organisms, semiochemicals (attractants), botanicals and "other plant protection 

substances of natural origin". 

This study was complemented by an analysis of specific uses of products commercialized in 

four countries of the EU (France, Germany, Spain and the United Kingdom). A fifth country, 

Switzerland was included in the study for comparison, because it has not been restricted by the 

implementation of Directive 91/414/EEC (superceded in June 2011 by EC regulation No 

1107/2011) until recently. For each country, official national online databases on authorised plant 

protection products (Table 10) were screened for authorised biocontrol active substances: 

Table 10: Consulted sources of information on authorized biocontrol plant protection products in 

five European countries: 

Country Official source / website Reference date 

France 

e-phy database of the Ministry of Agriculture & Fisheries 

http://e-phy.agriculture.gouv.fr 

31/8/2009 

Germany 

Online-Datenbank Pflanzenschutzmittel of the Federal Office of Consumer 

Protection and Food Safety (BVL) 

http://www.bvl.bund.de/DE/04_Pflanzenschutzmittel/01_Aufgaben/02_Zulassung 

12 /8/2009 

PSM/01_ZugelPSM/01_OnlineDatenbank/psm_onlineDB_node.html 

Spain 

Registro de productos Fitosanitarios of the Ministerio de Ambiente y Medio Rural 

y Marino 

http://www.mapa.es/es/agricultura/pags/fitos/registro/menu.asp 


Plant protection index ("Pflanzenschutzmittelverzeichnis") of the Federal Office 

for Agriculture (BWL, Fachbereich Pflanzenschutzmittel) 

31/7/2009 

http://www.psa.blw.admin.ch/index_de_5_2_A.htm 

Pesticides Register of UK approved products under the responsibility of the 

United 

Chemicals Regulation Directorate Pesticides 

Kingdom 

https://secure.pesticides.gov.uk/pestreg/ProdSearch.asp 

4/2009 

34

Chapter 4 

The survey was limited to uses concerning seven crops or cropping groups which are subject to 

ENDURE case studies: pomefruit (apples and pears), grapevine, cereals, rape, maize, potatoes and 

tomatoes (greenhouse and field), the latter being extended to other vegetables where deemed of 

interest. Country lists of representative products (generally up to two) were created and sorted 

according to uses in crops, target pests and pathogens were identified by English and scientific 

names wherever possible. 

Biocontrol substances registered on Annex 1 of the EU (Pesticides Database) 

The complete list compiled from data retrieved in April 2009 in the EU Pesticides Database is 

presented in Appendix 10. Excerpts concerning the four categories of substances compatible with 

biological control are presented in Table 11. 

Botanicals 

Botanicals are plant-substances resulting from simple processing e.g. pressing or from extraction. 

By extension the definition applies to a small numbers of compounds or even single ones extracted 

from plants and purified e.g. laminarine. 

Fourteen botanicals have been identified (Table 11) including two borderline cases for which 

single molecules identical to naturally occurring substances have been synthesised. 

- Four botanicals are authorised as repellents only: Extract from the tea tree, garlic extract, clove 

oil (plant oils) and pepper. 

- Six botanicals enter into the category of plant growth regulators. 

- The phytohormones gibberellic acid and gibberelline are botanicals produced in fermenters 

acting on plant growth. Spearmint oil and sea-alga extract are listed for their effect on plant 

growth as well. 

- The phytohormone ethylene is naturally present in plants and in soil and can be included here 

although it is typically produced in the petrochemical industry by steam cracking. 

- Carvone is a terpene produced by aromatic plants in particular by the mint. It can also be 

classified among the botanicals. To obtain a pure grade it is generally synthesised. In plant 

protection it is used as a growth regulator. 

- Laminarin is extracted from sea weed and is classified as elicitor. Rape seed oil enters into the 

category of insecticides/acaroids. Citronella oil is the only BCA approved as herbicide. 

- Pyrethrins are extracted from Pyrethrum flowers, from cultivars of Chrysanthemum 

cinerariaefolium. By their origin they are botanicals but their structures are analogous and their 

properties are similar to those of synthetic pyrethroids. Due to their mode of action which is 

analogous to conventional insecticides and their toxicity for aquatic and other non target 

organisms, they are not typical biological substances although they are accepted in organic 

farming. 

35

Heilig et al. 

Table 11: Active substances suitable for biological control listed on Annex I of 91/414/EEC (EU 

Pesticide Database) - Status on 21 April 2009 

Substance Category 1, 2 List 3 Inclusion Date Expiry Date 

Legislati 

on 

Botanicals 

Extract from tea tree RE A 4 01/09/2009 31/08/2019 2008/127 

Garlic extract RE A 4 01/09/2009 31/08/2019 2008/127 

Gibberellic acid PG A 4 01/09/2009 31/08/2019 2008/127 

Gibberellin PG A 4 01/09/2009 31/08/2019 2008/127 

Laminarin EL C 01/04/2005 31/03/2015 05/3/EC 

Pepper RE A 4 01/09/2009 31/08/2019 2008/127 

Plant oils / Citronella oil HB A 4 01/09/2009 31/08/2019 2008/127 

Plant oils / Clove oil RE A 4 01/09/2009 31/08/2019 2008/127 

Plant oils / Rape seed oil IN, AC A 4 01/09/2009 31/08/2019 2008/127 

Plant oils / Spearmint oil PG A 4 01/09/2009 31/08/2019 2008/127 

Sea-algae extract (formerly sea-algae extract and PG A 4 01/09/2009 31/08/2019 2008/127 

seaweeds) 

Botanicals copied by synthesis (s) or excluded (e) 

Carvone (s) PG C 01/08/2008 31/07/2018 2008/44/ 

EC 

Ethylene (s) PG A 4 01/09/2009 31/08/2019 2008/127 

Pyrethrins (e) IN A 4 01/09/2009 31/08/2019 2008/127 

Microbials 

Ampelomyces quisqualis strain AQ10 FU C 01/04/2005 31/03/2015 05/2/EC 

Bacillus subtilis str. QST 713 BA, FU C 01/02/2007 31/01/2017 07/6/EC 

Bacillus thuringiensis subsp. aizawai (ABTS-1857 and [IN] A 4 01/01/2009 31/12/2018 2008/113 

GC-91) 

Bacillus thuringiensis subsp. israelensis (AM65-52) [IN] A 4 01/01/2009 31/12/2018 2008/113 

Bacillus thuringiensis subsp. kurstaki (ABTS 351, PB [IN] A 4 01/01/2009 31/12/2018 2008/113 

54, SA 11, SA12 and EG 2348) 

Bacillus thuringiensis subsp. tenebrionis (NB 176) [IN] A 4 01/01/2009 31/12/2018 2008/113 

Beauveria bassiana (ATCC 74040 and GHA) IN A 4 01/01/2009 31/12/2018 2008/113 

Coniothyrium minitans FU C 01/01/2004 31/12/2013 03/79/EC 

Cydia pomonella granulosis virus (CpGV) [IN] A 4 01/01/2009 31/12/2018 2008/113 

Gliocladium catenulatum strain J1446 FU C 01/04/2005 31/03/2015 05/2/EC 

Lecanicillimum muscarium (Ve6) (former Verticillium IN A 4 01/01/2009 31/12/2018 2008/113 

lecanii) 

Metarhizium anisopliae (BIPESCO 5F/52) IN A 4 01/01/2009 31/12/2018 2008/113 

Paecilomyces fumosoroseus Apopka strain 97 [IN] C 01/07/2001 30/06/2011 01/47/EC 

Paecilomyces lilacinus [IN] C 01/08/2008 31/07/2018 2008/44/ 

EC 

Phlebiopsis gigantea (several strains) FU A 4 01/01/2009 31/12/2018 2008/113 

Pseudomonas chlororaphis strain MA342 FU C 01/10/2004 30/09/2014 04/71/EC 

Pythium oligandrum (M1) FU A 4 01/01/2009 31/12/2018 2008/113 

Spodoptera exigua nuclear polyhedrosis virus FU C 01/12/2007 30/11/2017 07/50/EC 

Streptomyces K61 (K61) (formerly Streptomyces FU A 4 01/01/2009 31/12/2018 2008/113 

griseoviridis) 

Trichoderma aspellerum (ICC012) (T11) (TV1) FU A 4 01/01/2009 31/12/2018 2008/113 

(formerly T. harzianum) 

Trichoderma atroviride (IMI 206040) (T 11) (formerly FU A 4 01/01/2009 31/12/2018 2008/113 

Trichoderma harzianum) 

Trichoderma gamsii (formerly T. viride) (ICC080) FU A 4 01/01/2009 31/12/2018 2008/113 

Trichoderma harzianum Rifai (T-22) (ITEM 908) FU A 4 01/01/2009 31/12/2018 2008/113 

Trichoderma polysporum (IMI 206039) FU A 4 01/01/2009 31/12/2018 2008/113 

Verticillium albo-atrum (WCS850) (formerly 

Verticillium dahliae) 

FU A 4 01/01/2009 31/12/2018 2008/113 

36

Chapter 4 


Other Natural 

Abamectin (aka avermectin) AC, IN A 3 01/01/2009 31/12/2018 2008/107 

Acetic acid HB A 4 01/09/2009 31/08/2018 2008/127 

Aluminium silicate (aka kaolin) RE A 4 01/09/2009 31/08/2019 2008/127 

Blood meal RE A 4 01/09/2009 31/08/2019 2008/127 

Carbon dioxide IN, RO A 4 01/09/2009 31/08/2019 2008/127 

Fat distilation residues RE A 4 01/09/2009 31/08/2019 2008/127 

Ferric phosphate MO C 01/11/2001 31/10/2011 01/87/EC 

Kieselguhr (diatomaceous earth) IN A 4 01/09/2009 31/08/2019 2008/127 

Milbemectin IN, AC C 01/12/2005 30/11/2015 05/58/EC 

Quartz sand RE A 4 01/09/2009 31/08/2019 2008/127 

Spinosad IN C 01/02/2007 31/01/2017 07/6/EC 

Other Natural, produced by synthesis 

Benzoic acid BA, FU, OT C 01/06/2004 31/05/2014 04/30/EC 

Potassium hydrogen carbonate FU A 4 01/09/2009 31/08/2019 2008/127 

Urea IN A 4 01/09/2009 31/08/2019 2008/127 

Other Natural, fatty acid 

Capric acid (CAS 334-48-5) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Caprylic acid (CAS 124-07-2) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Fatty acids C7 to C20 IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Fatty acids C7-C18 and C18 unsaturated potassium IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

salts (CAS 67701-09-1) 

Fatty acids C8-C10 methyl esters (CAS 85566-26-3) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Lauric acid (CAS 143-07-7) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Methyl decanoate (CAS 110-42-9) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Methyl octaonate (CAS 111-11-5) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Oleic acid (CAS 112-80-1) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Pelargonic acid (CAS 112-05-0) IN, AC, HB, PG A 4 01/09/2009 31/08/2019 2008/127 

Other Natural, repellent 

Calcium carbonate RE A 4 01/09/2009 31/08/2019 2008/127 

Limestone RE A 4 01/09/2009 31/08/2019 2008/127 

Methyl nonyl ketone RE A 4 01/09/2009 31/08/2019 2008/127 

Sodium aluminium silicate RE A 4 01/09/2009 31/08/2019 2008/127 

Repellents by smell/Fish oil RE A 4 01/09/2009 31/08/2019 2008/127 

Repellents by smell/Sheep fat RE A 4 01/09/2009 31/08/2019 2008/127 

Semiochemical 

(Z)-13-Hexadecen-11yn-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(Z,Z,Z,Z)-7,13,16,19-Docosatetraen-1-yl isobutyrate AT A 4 01/09/2009 31/08/2019 2008/127 

Ammonium acetate AT A 4 01/01/2009 31/12/2018 2008/127 

Hydrolysed proteins IN A 4 01/09/2009 31/08/2019 2008/127 

Putrescine (1,4-Diaminobutane) AT A 4 01/09/2009 31/08/2019 2008/127 

Trimethylamine hydrochloride AT A 4 01/09/2009 31/08/2019 2008/127 

Straight Chain Lepidoptera Pheromones AT A 4 01/09/2009 31/08/2019 2008/127 

37

Heilig et al. 


Semiochemical / SCLP 

(2E, 13Z)-Octadecadien-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(7E, 9E)-Dodecadien 1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(7E, 9Z)-Dodecadien 1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(7Z, 11E)-Hexadecadien-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(7Z, 11Z)-Hexadecdien-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(9Z, 12E)-Tetradecadien-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(E)-11-Tetradecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(E)-5-Decen-1-ol AT A 4 01/09/2009 31/08/2019 2008/127 

(E)-5-Decen-1-yl-acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(E)-8-Dodecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(E,E)-8,10-Dodecadien-1-ol AT A 4 01/09/2009 31/08/2019 2008/127 

(E/Z)-8-Dodecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-11-Hexadecen-1-ol AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-11-Hexadecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-11-Hexadecenal AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-11-Tetradecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-13-Octadecenal AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-7-Tetradecenal AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-8-Dodecen-1-ol AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-8-Dodecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-9-Dodecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-9-Hexadecenal AT A 4 01/09/2009 31/08/2019 2008/127 

(Z)-9-Tetradecen-1-yl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

Dodecyl acetate AT A 4 01/09/2009 31/08/2019 2008/127 

Tetradecan-1-ol AT A 4 01/09/2009 31/08/2019 2008/127 

1 AC=acaricide, AT= attractant, BA=bactericide, EL=elicitor, FU=fungicide, HB=herbicide, IN=insecticida, MO=molluscicide, 

NE=nematicide, PA=Plant Activator, PG=Plant Growth, RE=repellent, RO=rodenticide. 

2 

Category in [ ] added by author 

3 

A: Existing active substances divided into four lists for phased evaluations; C: New active substances 

Micro-organisms 

The term micro-organism is defined in regulation (EC) No 1107/2009: ‘micro-organisms’ means 

any microbiological entity, including lower fungi and viruses, cellular or non-cellular, capable of 

replication or of transferring genetic material.. This definition applies to, but is not limited to, 

bacteria, fungi, protozoa, viruses and viroids. It does not include multicellular organisms, such as 

nematodes or insects. 

Twenty five microbial species are included in annex I, some of which are represented by 

several strains. Six bacterial (sub)species (Bacillus subtilis, Pseudomonas chlororaphis and four 

subspecies of Bacillus thuringiensis) and two virus species (Cydia pomonella Granulose Virus and 

Spodoptera exigua NPV) are included. All B.t. subspecies and viral agents are approved for insect 

control. Pseudomonas is approved for fungicidal seed treatments and Bacillus subtilis can be used 

against plant pathogenic fungi and bacteria. Seventeen fungal agents belonging to twelve genera are 

listed, Trichoderma being represented by five species. Beauveria bassiana, Lecanicillimum 

muscarium and Metarhizium anisopliae are approved for use as insecticides, the other fungal agents 

for use against fungal diseases. 

Semiochemicals (attractants) 

Semiochemicals are chemical substances such as pheromones, kairomones and allomones that act to 

modify the behaviour of pests or their natural enemies. 

In the table based on the EU Pesticides Database, Straight Chain Lepidopteran Pheromones (SCLP) 

are highlighted in green, non-SCLP-pheromones in light cyan and other attractants (including 

hydrolysed proteins) are highlighted in yellow. There is one repellent which is marked in light red. 

38

Chapter 4 

SCLPs are included in annex I as a group but 25 compounds of this group are also listed 

individually. In the inclusion directive 2008/127/EC, some molecules are mentioned three times, as 

an individual substance, in a blend of the same type, e.g. acetates and in mixed blends, e.g. alcohols 

and acetates. Often single SCLP compounds show attraction to one or more moth species and 

typically a combination of two or more of these compounds in a precise ratio enhances the 

attraction and the specificity. Thus SCLPs should be considered as a whole group and it must not be 

concluded that each compounds stands for one species. 

The SCLPs listed individually are typical examples found in the pheromone blends of moth 

pest species currently of economic importance. A large variety of compounds and isomers, an 

estimated number of about 300 identified molecules, used by Lepidopterans are not listed here. 

They differ in carbon chain length, in the number of double bonds and/or their positions and in their 

chemical functional group (alcohol, acetate or aldehyde). SCLPs can be used for mass trapping, 

mating disruption or in attract and kill devices (A&K) or formulations. When associated with an 

insecticide, i.e in A&K products, attractants do not need to be included in annex I. 

Two non SCLP pheromones, (Z)-13-Hexadecen-11yn-1-yl acetate and (Z,Z,Z,Z)-7,13,16,19- 

Docosatetraen-1-yl isobutyrate, as well as four semiochemicals other than pheromones attractive to 

different fly (Diptera) species are listed in the EU Pesticides Database: Ammonium acetate, 

hydrolysed proteins, putrescine (1,4-diaminobutane) and Trimethylamine hydrochloride. 

Other Plant Protection substances of natural origin 

This group has been created for the purpose of the survey. It includes mineral substances as well as 

substances produced by or derived from animals or from micro-organisms. Thus very diversified 

substances and products like limestone powder, kaolin as well as diatomaceous earth (Kieselguhr), 

fatty acids and their derivates (e.g. soaps) can be found in this group. Not all substances of this 

group do meet the expectation of low non-target toxicity and low environmental impact. 

Some active substances included in annex I are produced by micro-organisms. Spinosad which 

is produced by the bacterium Saccharopolyspora spinosa finds its place here; it is accepted for 

organic farming. Milbemectin is a mixture of natural compounds (milbemycins) isolated from 

fermentation broth of the fungus Streptomyces hygroscopicus subsp. aureolacrimosus. The 

substance is active against insects of different families and a large range of mites. Abamectin 

contains avermectins which are biosynthesised by Streptomyces avermitilis. The substance shows 

very high toxicity in Mammals and in aquatic organisms. Milbemectin and abamectin are not 

authorised in organic crop protection. 

Potassium hydrogen carbonate is a slightly basic substance used for its fungicidal properties. 

The US FDA considers this substance as GRAS (Generally Recognised as Safe). Six natural 

substances are specifically marked in the EU List, they are used as animal repellents: three are 

minerals (Calcium carbonate, limestone, sodium aluminium silicate), two are of animal origin (fish 

oil and sheep fat) while methyl nonyle ketone is either produced by synthesis or extracted from 

plant oils (rue). The latter repellent acts by its strong odour. It is naturally present in some edible 

crops and spices. 

Limit cases and exclusions 

With regards to their (eco)toxicological profile and environmental impact neither sulphur and its 

derivates (iron sulphate) nor cupric compounds i.e. Bordeaux mixture, copper hydroxide, copper 

oxichloride and cuprous oxide are considered here as typical biological substances although they 

might be accepted in organic agriculture. 

Tall oils (crude or pitch) are a by-product in the Kraft process used in the paper industry. Thus 

they are substances resulting from a chemical process and are classified as chemicals here. Calcium 

carbide is produced from lime and coke in electric arc furnaces. It is fitted among chemicals but is 

used as a repellent like some other minerals. 1-Methyl-cyclopropene is an inhibitor of the effects of 

39

Heilig et al. 

the phytohormone ethylene and is mainly used to conserve cut flowers. It is placed among the 

chemicals. 

Uses of biocontrol products in five European countries 

Registered plant protection substances 

In each country all BCAs authorised for uses in seven crops or cropping groups were identified. 

Lists of representative products (generally up to two) were created and sorted according to uses in 

crops: pomefruit (apples and pears), vine, cereals, rape, maize, potatoes and tomatoes (greenhouse 

and field), the latter was extended to other vegetables where deemed of interest. 

In France twelve different microbial BCA species (or sub-species in the case of Bacillus 

thuringiensis) are authorised among which two species, Beauveria tenella and Candida oleophila 

are not yet included in 91/414 Annex I. Only four botanical active substances are authorised, 

including rotenon (EU non-inclusion decision in April 2008 but temporary authorisation in FR) and 

pyrethrum which were excluded from our survey. Fenugreek extracts benefited from a specific 

French approach to plant extracts under former national rules, while EU approval was given in 

2010, after the survey. Laminarin is included in Annex I. Five Straight Chain Lepidopteran 

Pheromones (SCLP) blends or associations (one just specifying minor components used for the 

single target codling moth) are registered for mating disruption in orchards or vineyard. 

In Germany nine microbial BCAs are authorised in Plant Protection Products (all included). 

Only four botanical substances are listed for plant protection, two of which are included in Annex I 

(pyrethrins and rape seed oil), two are not (azadirachtin and lecithin). Three different SCLP 

associations are authorised for mating disruption against Codling Moth or Vine Moths. 

For Germany only fully registered BC products according to the rules of the PPP directive 

were included in the survey. As a consequence, plant strengtheners authorised according to the 

Federal Plant Protection Act §§ 31ff were excluded. Plant Strengtheners can avoid the EU 

procedures and requiremments for plant protection products but they must not claim specific 

protective properties either. 

In Spain ten microbial BCAs are authorised, all of which are included in EU Annex 1. Only 

three botanical substances could be identified: Pyrethrins and rotenon which are excluded from the 

survey and Azadirachtin (Neem extract) which was re-included in EU Annex I in 2011. The plant 

growth regulators gibberellinic acid/gibberellin are not explored in the survey. Only four SCLP 

associations are authorised for mating disruption in vine and orchards including two for oriental 

fruit moth and peach twig borer typical for peach orchards. 

In Switzerland twelve different microbial BCA species (or sub-species in the case of Bacillus 

thuringiensis) are authorised, among which is one species not included in 91/414 Annex I: 

Beauveria brognartii. Eleven botanicals are approved, among which the insecticides Pyrethrum 

(included in EU Annex I) and rotenon (rejected from Annex I) have been excluded from the survey 

because of their toxicological profile. The plant growth regulators gibberellic acid and gibberellin 

were also excluded from the survey. Five substances not included in EU Annex I are authorised: 

Azadirachtin (Neem extract), fennel oil, lecithin, mustard powder and Quassia extract. An 

impressive number of semiochemicals, eleven different SCLP associations are authorized for 

mating disruption allowing the control a large variety of moths in orchards (including one 

association of 8 compounds against five different species) and vineyards. This can be related to the 

facilitated approval of pheromone products in Switzerland. 

In the UK eight microbial BCAs are approved but only a single botanical (Laminarin, EU 

approved) and a single pheromone blend (for codling moth). No biological plant protection products 

are available for use in grapevine, rape, maize or potatoes. With regard to the global availability of 

biological control products in the different crops, pomefruit, vegetables and vine are generally in a 

better position than arable crops in the countries included in the survey. In the UK e.g. only 

40

Chapter 4 

laminarin is available on wheat and cereals, and no biological plant protection products are 

registered for rape, maize or potatoes. 

None of the EU Member States covered in the present survey shows such a variety of BCAs as 

Switzerland where we find the largest numbers of microbials, botanicals and pheromone blends 

authorised in the crops subject of the inquiry. Only France reaches the number of twelve microbial 

BCAs in registered products. The privileged situation in the Helvetic Confederation can be 

explained by the flexible regulatory approach of the competent authorities in the past, until the 

progressive implementation of EU directive 91/414/EEC and the related framework, as well as the 

sustained support by experts in confederal agronomic institutes. 

Invertebrate biocontrol agents 

Invertebrate biocontrol agents (BCAs) used in the five European countries of this survey are listed 

in Appendix 11. 

In France invertebrate BCAs cannot be registered and they do not yet need to be formally 

declared, but a law passed on 12 th July 2010 created the basis to establish rules governing the 

introduction into the environment of non-indigeneous macro-organisms useful to plants. Procedures 

and requirements for authorisations which will also cover non-indigeneous beneficial are expected 

to be set up for the in the coming months. The list provided in the present survey is based on the 

voluntary declarations to ACTA by the producers wishing to have their beneficials published in the 

non-official Index Phytosanitaire. 

Invertabrate BCAs must be registered in Germany. An official list which is regularly updated 

is published by the Julius Kühn Institute. 

In Spain companies which are responsible of commercialisation of IBCAs must give 

information to the Ministry of Agriculture to allow the inscription into a register before 

commercialisation (Orden APA/1470/2007). This information given is about name of commercial 

product, identification of the organism, the manufacturer, the company responsible for 

commercialisation. Another law (43/2002; 20 th of November 2002) covers the introduction of exotic 

organisms (article 44). 

In Switzerland invertebrate BCAs must be formally approved by the BLW (Bundesamt für 

Landwirtschaft) and they are listed together with the plant protection products. 

In the United Kingdom no authorisation is required to release indigenous beneficials but the 

import (and release) of non indigenous species must be approved by the Advisory Committee for 

the Release of Exotics (ACRE acting under DEFRA). 

41

Chapter 5 


1. Regulatory aspects 

Ulf Heilig 1 , Claude Alabouvette 2* and Bernard Blum 1 

1 International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel, 


2 INRA, UMR1229, Microbiologie du Sol et de l'Environnement, 17 rue Sully, F -21000 Dijon, 

France 

Objectives 

The objective of the work was to identify typical hurdles for the placing of biological plant 

protection products on the market experienced by biocontrol industry or evaluators in the recent 

past under the European directive 91/414/EEC. In parallel, we examined the new regulation (No 

1107/2009/EC of the European Parliament and of the Council of 21 October 2009) concerning the 

placing of plant protection products on the market and repealing Council Directives 79/117/EEC 

and 91/414/EEC and the new directive (N° 2009/128/EC of the European Parliament and of the 

Council of 21 October 2009) establishing a framework for Community action to achieve the 

sustainable use of pesticides. These two texts were examined for provisions creating new 

opportunities for the approval biocontrol agents, their placing on the market and use. In fine, it was 

the intent to establish a dialogue with EU regulators and evaluators in European institutions, i.e. in 

the European Commission and in the European Food Safety Agency (EFSA) and to seek solutions 

in common for the problems encountered. 

Working method 

An ad hoc group of representatives from the biocontrol industry and INRA called "Regulatory 

Review Team" was set up. Two full-day working sessions were organised in which regulatory 

experts identified difficulties and questions but also described positive experience and perspectives. 

The work of the Regulatory Review Team active under Reasearch Activity RA4.3 of the 

ENDURE network was then summarised and reported in a meeting of a delegation of ENDURE 

partners (IBMA, INRA and ACTA) with representatives of the European Commission (DG 

SANCO, DG Agriculture, DG Research) and the EFSA in Brussels (24 September 2009). 

Results 

A PowerPoint presentation entitled "Gaps - Problems - Opportunities for BCAs in E.U. 

Regulation - From Past to Future" was prepared for the ENDURE – Commission meeting, with 

inputs on general regulatory issues, micro-organisms, straight chain lepidopteran pheromones and 

botanicals. In this document, two key issues related to directive 2001/36/EC annex II B which fixed 

requirements for microbial active substances were highlighted. Readers may note that since 14 th 

June 2011 Regulation (EU) No 544/2011 implements these data requirements unchanged to reg. 

* Current address: AGRENE, 47 rue Constant Pierrot 21000 DIJON, c.ala@agrene.fr 

42

Chapter 5 

(EC) No 1109/2009. Tests suggested by evaluation experts and intended to establish the genetic 

stability of a strain do not reflect practical conditions, while in the case of potential microbial 

contaminants no European reference list is available. The incidence of many pathogens can be 

excluded by production methods or the geographic location of production sites. Tolerance limits for 

contamination levels could take into consideration thresholds used in food industry, application 

levels for the microbial product and naturally occurring background levels. The two issues 

presented here but also other examples put forward to the Regulatory Review Team lead to the 

statement that "not all the studies or tests that can be performed for microbials will necessarily 

yield relevant data". 

The most important experience with semiochemicals was made during the on-going reassessment 

of Straight Chain Lepidopteran Pheromones (SCLPs), which were supported by an 

IBMA Task Force. Regulators and evaluators were flexible in accepting a single common dossier 

for all compounds notified but although an OECD guidance document recommends data waiving 

for numerous SCLP requirements, the Rapporteur Member State insisted that all existing data and 

study reports on all compounds be submitted on the grounds that the requirements of the directive 

are superior to the guidance document recommendations. So far, the re-assessment procedure 

resulted in the inclusion with postponed peer review of SCLPs as a group, but 25 substances are 

also listed individually. New substances can be included in a simplified procedure provided that the 

applicant has access to the existing dossier. Remaining questions include what industry input will 

be required during the peer review by EFSA, the E.U. status of a revised OECD guidance document 

for semiochemicals other than SCLPs, the decision if MRLs are required for sprayable SCLP 

formulations, and equivalence criteria for SCLP substances. It was also noted that under the 

Biocidal Product Directive, rules and fees applied to SCLPs created an economic hurdle which 

resulted in the submission of a dossier for only one compound. 

Extracts from plants - as long as not purified - consist of mixtures of molecules while data 

requirements of directive 91/414/EEC maintained under new regulation (EC) No 1107/2009 are 

basically designed for defined single substances. Thus those requirements often do not fit for 

mixtures of several substances. It must be decided if the most “active” substance, the one with the 

highest content in the extract or the whole extract shall be used in studies required for different 

sections of a dossier i.e. for data on physical-chemical properties, metabolism, toxicology, residues, 

environmental fate and behaviour, and which data shall be used in risk assessment. While the whole 

extract can be recommended for use in toxicity studies, it is not convenient for residue, metabolism 

or environmental studies because in practice it is generally not possible to determine the fate of all 

compounds contained in an extract. Questions asked by evaluators from several Member States 

after the issuing of a draft assessment report for Neem extract and its lead substance Azadirachtin A 

illustrate the difficulties experienced by an applicant in the evaluation process for a botanical. 

Regulation (EC) No 1107/2009 concerning the placing of plant protection products on the 

market provides for a specific status for "low risk active substances" (article 22). Many biocontrol 

substances can be expected to qualify for this new category but one exclusion criterion, the half-life 

in soil, may cause problems for microbial active substances unless it is clearly limited to chemicals. 

A full set of data is required to gain the status of low risk active substance but products containing 

them exclusively and without co-formulants of concern will benefit from reduced dossier 

requirements and time lines for approval. Micro-organisms, plant extracts or other natural 

substances may also meet the criteria for "Basic substances" provided for in article 23 but the 

discussion in the ENDURE-Commission meeting made it clear that this category is without interest 

for manufacturers who intend to market their substances for plant protection. It was noted that the 

new regulation does not provide for generic waivers i.e. for justifications of non submission of data 

or exemptions from requirements for groups of substances or products. 

43

Heilig et al. 

In the sustainable use directive 2009/128/EC a number of provisions in favour of biological 

pest control measures or non-chemical methods have been identified. The new regulation also 

mentions in recital 35 that priority should be given to "non-chemical and natural alternatives 

wherever possible" but since the definition of non-chemical methods refers to "physical, mechanical 

or biological pest control" and does not specifically mention microbials, semiochemicals, botanicals 

or other natural substances with non-toxic mode of action it must be clarified how those groups are 

covered by the definition. 

Conclusion 

In the meeting between the ENDURE delegation and representatives of the European 

Commission, the need for discussions between regulators, evaluators and industry about 

requirements especially those relevant for microbial and botanical substances was recognised. 

Article 77 of the new plant protection product regulation authorises the Commission to "adopt or 

amend technical and other guidance documents e.g. explanatory notes or guidance documents on 

the content of the application concerning micro-organisms, pheromones and biological products." 

Thus at least part of the problems experienced by applicants can be addressed in guidance 

documents. Industry representatives and companies directly concerned by evaluations or reviews of 

biocontrol agents should enter into discussions with evaluators (EFSA or Competent Authorities in 

Member States) without forgetting the leading role of the Commission. Industry should fix 

priorities, prepare rationales and make substantiated proposals dealing with data requirements 

considered inappropriate, unnecessary or unrealistic. 

44

Chapter 6 


2. Technical aspects: factors of efficacy 

Michelina Ruocco 1 , Sheridan Woo 1,2 , Francesco Vinale 1 , Stefania Lanzuise 2 , Matteo Lorito 1,2 

1 CNR-IPP, Consiglio Nazionale delle Ricerche, Istituto per la Protezione delle Piante, via 

Università 133, 80055 Portici, Italy 

2 Dip. Arboricoltura, Botanica e Patologia Vegetale, Università di Napoli Federico II, via 

Università 100, 80055 Portici, Italy 

Quality of the BCAs formulations 

Numerous investigations on the development of biopesticides have been initiated as legislation and 

government policy have demanded less reliance on chemical pesticides and greater adoption of 

IPM. In Europe, some countries have set goals of reducing pesticide use by 50%. Successes have 

been achieved through better timing of applications, so that lower dosages are effective and 

substituting less hazardous and more active materials, to reduce the number of applications. 

Biopesticides are distinguished from conventional chemical pesticides as many are very 

selective and are non-toxic towards non-target organisms. While biopesticides are likely to be less 

harmful to the environment than the conventional ones, care needs to be taken that wastage is 

minimised, by selecting the most appropriate droplet spectrum. A disadvantage of biological agents 

relative to chemicals, is that many are not sufficiently persistent and are relatively slow acting; 

therefore, research has been directed at extending the period of activity. However, some such agents 

may persist in the field or the forest for many months, and a risk–benefit analysis should be 

performed to establish their environmental acceptability. 

Transition from the optimised conditions of a laboratory experiment to the harsh conditions 

experienced in the field has so far proved more difficult for application of biopesticides in contrast 

to chemicals. This has undoubtedly been due to lack of investment in the development of effective 

formulations and delivery systems, in order to commercialise more potential biopesticides. The 

relatively small effort invested in target-specific sprayers, compared with the investment in 

laboratory studies, has led to unbalanced development, and exemplifies the need for closer 

integration between formulation and engineering research. The challenge is to get effective 

formulations so that biological control agents can be easily applied by farmers. 

A good example, the case of Trichoderma: direct and indirect mode of action against 

plant pathogens 

Trichoderma species have long been recognized as biological control agents (BCAs) for the control 

of plant disease and for their ability to increase plant growth and development. They are widely 

used in agriculture, and some of the most useful strains demonstrate a property known as 

‘rhizosphere competence’, the ability to colonize and grow in association with plant roots (Harman 

2000). Much of the known biology and many of the uses of these fungi have been documented 

recently (Harman et al. 2004a; Kubicek et al. 1998; Perello et al. 2009). The taxonomy of this 

fungal genus is continually being revised, and many new species are being described (Komon- 

Zelazowska et al. 2007; Kubicek et al. 2008; Overton et al. 2006; Samuels 2006; Samuels and 

45

Ruocco et al. 

Ismaiel 2009). The mechanisms that Trichoderma uses to antagonize phytopathogenic fungi include 

competition, colonization, antibiosis and direct mycoparasitism (Harman 2006, 2011; Howell 

2003). This antagonistic potential serves as the basis for effective biological control applications of 

different Trichoderma strains as an alternative method to chemicals for the control of a wide 

spectrum of plant pathogens (Harman et al. 1991; Lorito et al. 2010). 

The colonization of the root system by rhizosphere competent strains of Trichoderma results in 

increased development of root and/or aerial systems and crop yields (Bae et al. 2011; Chacon et al. 

2007; Kubicek et al. 1998; Yedidia et al. 2003). Trichoderma has also been described as being 

involved in other biological activities such as the induction of plant systemic resistance (Shoresh et 

al. 2010; Tucci et al. 2011) and antagonistic effects on plant pathogenic nematodes (Jegathambigai 

et al. 2008; Sharon et al. 2001).Some strains of Trichoderma have also been noted to be aggressive 

biodegraders in their saprophytic phases, in addition to acting as competitors to fungal pathogens, 

particularly when nutrients are a limiting factor in the environment (Worasatit et al. 1994). These 

facts strongly suggest that in the plant root environment Trichoderma actively interacts with the 

components in the soil community, the plant, bacteria, fungi, other organisms, such as nematodes or 

insects, that share the same ecological niche (Lorito et al. 2010). 

Trichoderma spp. are important participants in the nutrient cycle. They aid in the 

decomposition of organic matter and make available to the plant many elements normally 

inaccessible. Yedidia et al. (2001) noted that the presence of the fungus increased the uptake and 

concentration of a variety of nutrients (copper, phosphorus, iron, manganese and sodium) in the 

roots of plants grown in hydroponic culture, even under axenic conditions. These increased 

concentrations indicated an improvement in plant active-uptake mechanisms. Corn that developed 

from seeds treated with T. harzianum strain T-22 produced higher yields, even when a fertilizer 

containing 40% less nitrogen was applied, than the plants developed from seed that was not treated 

with T-22 (Harman 2000). This ability to enhance production with less nitrate fertilizer, provides 

the opportunity to potentially reduce nitrate pollution of ground and surface water, a serious adverse 

consequence of large-scale maize culture. In addition to effects on the increase of nutrient uptake 

and the efficiency of nitrogen use, the beneficial fungi can also solubilize various nutrients in the 

soil, that would be otherwise unavailable for uptake by the plant (Altomare et al. 1999b). 

The cross-talk that occurs between the fungal BCA and the plant is important both for 

identification of each component to one another and for obtaining beneficial effects. Somehow, the 

plant is able to sense, possibly by detection of the released fungal compounds, that Trichoderma is 

not a hostile presence, therefore the plant defence system is not activated as it is when there is pest 

attack and the BCA is recognized as a plant symbiont rather than a plant pathogen (Woo and Lorito, 

2006). Molecules produced by Trichoderma and/or its metabolic activity also have potential for 

promoting plant growth (Chacón et al., 2007; Vinale et al. 2008a; 2008b; Yedidia et al. 1999). 

Applications of T. harzianum to seed or the plant resulted in improved germination, increased plant 

size, augmented leaf area and weight, greater yields (Altomare et al. 1999a; Harman et al. 2004c, b; 

Inbar and Chet 1995; Tucci et al. 2011; Vinale et al. 2008a). 

Numerous studies indicated that metabolic changes occur in the root during colonization by 

Trichoderma spp., such as the activation of pathogenesis-related proteins (PR-proteins), which 

induce in the plant an increased resistance to subsequent attack by numerous microbial pathogens 

(Table 12) 

46

Chapter 6 

Table 12: Evidence for, and effectiveness of, induced resistance in plants by Trichoderma 

species (Harman et al., 2004a). 

The induction of systemic resistance (ISR) observed in planta determines an improved control 

of different classes of pathogens (mainly fungi and bacteria), which are spatially and temporally 

distant from the Trichoderma inoculation site. This phenomenon has been observed in many plant 

species, both dicotyledons (tomato, pepper, tobacco, cotton, bean, cucumber) and monocotyledions 

(corn, rice). For example, Trichoderma induces resistance towards Botrytis cinerea in tomato, 

tobacco, lettuce, pepper and bean plants, with a symptom reduction ranging from 25 to 100% (Tucci 

et al. 2011). Moreover, Trichoderma determined an overall increased production of defence-related 

plant enzymes, including various peroxidases, chitinases, β-1,3-glucanases, and the lipoxygenasepathway 

hydroperoxide lyase (Harman et al. 2004c; Howell et al. 2000; Yedidia et al. 1999) of T. 

harzianum strain T-39, the active ingredient of the commercial product TricodexTM. 

Thus far, Trichoderma is able not only to produce toxic compounds with a direct antimicrobial 

activity against pathogens, but also to generate fungal substances that are able to stimulate the plant 

to produce its own defence metabolites. In fact, the ability of T. virens to induce phytoalexin 

accumulation and localized resistance in cotton has already been discussed (Hanson and Howell 

2004). In cucumber, root colonization by strain T-203 of T. asperellum caused an increase in 

phenolic glucoside levels in the leaves; the aglycones, which are phenolic glucosides with the 

carbohydrate moieties removed, are strongly inhibitory to a range of bacteria and fungi (Yedidia et 

al. 2003). 

47

Ruocco et al. 

A fundamental part of the Trichoderma antifungal capability consists in the production and 

secretion of a great variety of extracellular cell wall degrading enzymes (CWDEs), including 

endochitinases, β-N-acetylhexosaminidase (N-acetyl-β-D-glucosaminidase), chitin-1,4-β-chitobiosidases, 

proteases, endo- and exo-β-1,3-glucanases, endo β-1,6-glucanases, lipases, xylanases, 

mananases, pectinases, pectin lyases, amylases, phospholipases, RNAses, DNAses, etc. (Benitez et 

al. 2004; Lorito et al. 1998). The chitinolytic and glucanolytic enzymes are especially valuable for 

their CWDE activity on fungal plant pathogens, hydrolyzing polymers not present in plant tissues 

(Woo et al. 1999). Each of these classes of enzymes contains diverse sets of proteins with distinct 

enzymatic activities. Some have been purified, characterized and their encoding genes cloned (Ait- 

Lahsen et al. 2001; de la Cruz et al. 1992; 1995a; 1995b; Garcia et al. 1994; Limon et al. 1995; 

Lora et al. 1995; Lorito et al. 1993,. 1994b; Montero et al. 2007; Peterbauer et al. 1996; Suarez et 

al. 2004; Viterbo et al. 2001, 2002). Once purified, many Trichoderma enzymes have shown to 

have strong antifungal activity against a wide variety of phytopathogens, and they are capable of 

hydrolyzing not only the tender young hyphal tips of the target fungal host, but they are also able to 

degrade the hard, resistant conservation structures such as sclerozi. 

Trichoderma spp. have been widely studied, and are presently marketed as biopesticides, 

biofertilizers and soil amendments, due to their ability to protect plants, enhance vegetative growth 

and contain pathogen populations under numerous agricultural conditions (Harman 2000, 2004; 

Vinale et al. 2008b). The commercial success of products containing these fungal antagonists can 

be attributed to the large volume of viable propagules that can be produced rapidly and readily on 

numerous substrates at a low cost in diverse fermentation systems. The living microorganisms, 

conserved as spores, can be incorporated into various formulations, liquid, granules or powder etc., 

and stored for months without losing their efficacy (Jin et al. 1996). To date more than 50 different 

Trichoderma-based preparations are commercialized and used to protect or increase the 

productivity of numerous horticultural and ornamental crops (Table 13; Lorito et al. 2006). 

The case Trichoderma: mode of application, persistence on the target and new 

formulations. 

Effectiveness under controlled conditions (even under field conditions) does not necessarily 

guarantee that the organism will perform successfully; proper formulation is a prime condition for 

meeting market requirements. For instance an efficient biocontrol agent of soilborne and airborne 

pathogens must first and foremost protect the young seedling against detrimental attack by infective 

inoculum. Therefore some factors may be considered: 

(a) soil ecosystem factors such as moisture, pH, structure, and temperature; 

(b) root colonization capacity; 

(c) reasonable shelf life; 

(d) efficiency of application of the biocontrol agent in terms of its specific habitat and target 

(Spiegel and Chet 1998) 

48

Table 13: Trichoderma-based preparations commercialized for biological control of plant diseases. 

Chapter 6 

Commercial 


Product 

Formulation, 

Uses - Location, 

Uses, Pathogens 

Manufacturer/Supplier, Country, Internet Reference 

Product 

Organism(s) 

Type 

Application 

Crops 

controlled 

Ago Biocontrol 

Trichoderma 

50 

T. harzianum Biological 

fungicide 

n/a 

Flowers, vegetables, 

fruits, other crops 

Fusarium, Rhizoctonia, 

Alternaria, Rosellinia, 

Botrytis, Sclerotium, 

Phytophthora spp 

Ago Biocontrol, Colombia 

(http://www.sipweb.org/directorymcp/fungi.html) 

Antagon 

Binab T 

Trichoderma 

spp. 

T. harzianum, 

T. polysporum 

Biological 

fungicide 

Biological 

fungicide 

BioFit T. viride Biological 

fungicide 

Bio-Fungus 

(formerly 

Anti-Fungus), 

Supresivit 

Trichoderma 

spp. 

Biological 

fungicide 

powder 

Pellets, wettable 

powder or 

granules; spray, 

drench, mixed in 

soil 

Seed treatment, 

root/tuber dip, 

drench; Used 

alone or in 

combination with 

chemicals. 

granular, wettable 

powder, sticks, 

crumbles; soil 

incorporation; 

spray or injection 

Horticulture 

(commercial), parks, 

recreational areas, 

sports fields 

Wood products; 

ornamental, shade, 

forest trees; 

greenhouse, nursery, 

field; cut flowers, 

potted plants, 

vegetables, 

mushrooms, flower 

bulbs 

Gram, pepper, 

groundnut, wheat, 

potato, ginger, 

turmeric, peas, 

matki, mung, urid , 

tomato, bhindi, 

onion, other 

vegetables, grapes. 

Flowers, 

strawberries, trees, 

vegetables 

damping-off diseases 

Wood rots causing 

internal decay, or 

originating from pruning 

wounds; Didymella, 

Chondrostereum, 

Heterobasidion, Botrytis, 

Verticillium, Pythium, 

Fusarium, Phytophthora, 

Rhizoctonia 

Pythium, Rhizoctonia, 

Fusarium, Sclerotium, 

other root rots; for 

Botrytis in combination 

with chemicals 

Sclerotinia, 

Phytophthora, 

Rhizoctonia solani, 

Pythium spp., Fusarium, 

Verticillium 

De Ceuster Meststoffen N.V. (DCM), Belgium 

(http://www.agroBiologicals.com/products/P1609.htm) 

BINAB Bio-Innovation AB, Sweden 

(http://www.algonet.se/~binab/index2.html); Henry 

Doubleday Research Association, United Kingdom; 

Svenska Predator AB, Sweden; E.R. Butts International, 

Inc., USA 

Ajay Bio-tech (India) Ltd., India 

(http://www.ajaybio.com) 

BioPlant, Denmark (www.bioplant.dk); De Ceuster 

Meststoffen N.V. (DCM), Belgium 

49

Ruocco et al. 

Table 13 (continued): 

Trichoderma-based preparations commercialized for biological control of plant diseases. 

Commercial 

Product 


Organism(s) 

Product 

Type 

Formulation, 

Application 

Uses - Location, 

Crops 

Uses, Pathogens controlled 

Manufacturer/Supplier, Country, Internet Reference 

Combat 

T. harzianum, 

T. virens 

(=T. lignorum 

G. virens), 

Bacillus 

subtilis 

Biological 

fungicide 

Talc; seed 

treatment, 

broadcast, root 

dip, drench, 

foliar spray 

Grapes, cotton, 

pulses, tea, potato, 

tomato, oil seeds, 

tobacco, spices, 

cereals, vegetables, 

horticultural crops 

Downy mildew, powdery 

mildew, die back, 

Verticillium, Fusarium, 

Panama wilt; pod, seedling, 

late blight; root, collar, stem, 

red, soft, clump, dry, bean, 

fruit, pod rot; black leg, 

damping off, abnormal leaf 

fall, black thread, canker 

BioAg Corporation USA 

(http://www.bioag.com/products.html) 

Harzian 20 

(under 

T. harzianum Biological 

fungicide 

n/a 

orchard crops, 

vineyards 

Armillaria spp., Pythium 

spp., Sclerotinia spp. 

Natural Plant Protection (NPP), France 

(http://www.agroBiologicals.com/products/P1362.htm) 

development) 

PlantShield T. harzianum Biological 

fungicide 

Primastop G. catenulatum Biological 

fungicide 

Granules, 

wettable powder; 

soil drench, 

foliar spray 

Powder; drench, 

spray, irrigation 

Greenhouse, 

flowers, 

ornamentals, 

herbs, nursery, 

vegetable crops; 

hydroponic, 

orchard trees 

ornamental, 

vegetable, tree 

crops 

Pythium, Fusarium, 

Rhizoctonia, 

Cylindrocladium, 

Thielaviopsis; suppresses 

Botrytis 

pathogens causing seed, root, 

stem rot, wilt disease 

BioWorks, Inc., USA 

(http://www.bioworksbiocontrol.com) 

Kemira Agro Oy, Finland (http://growhow.kemiraagro.com); 

AgBio Development Inc.USA 

Root Pro, 

RootProtato 

T. harzianum, 

T. cornedia 

Biological 

fungicide 

Powder; spores 

mixed with 

growing media 

Seedling, rooting 

stage in nursery; 

Horticulture - 

flowers, 

vegetables, 

potatoes 

Rhizoctonia solani, Pythium 

spp., Fusarium spp., 

Sclerotium rolfsii 

Mycontrol Ltd., Israel; Efal Agri, Israel 

(http://www.efal.com/main.htm, 

http://www.agroBiologicals.com/company/C1096.htm) 

50

Chapter 6 

Many preparations have been developed to ensure a good shelf life of the product based on 

Trichoderma. Some of that formulation are stable in terms of pH, that remains constant and low 

(5.5) during the entire growth period, thus preventing bacterial contamination. Moreover the shelf 

life of the fungus at 25 °C is 1 year and from 1 to 2 years, the number of colonies-forming-units 

(CFUs) decreases by one order of magnitude. Many of that formulation have been proven 

successful in several experiments in the greenhouse and field. The rapid mass production of 

promising antagonists in the form of spores, mycelia or mixtures of both, has been achieved by 

liquid-fermentation technology: mass production of biomasses of T. hamatum, T. harzianum, and T. 

viride was reached by utilizing commercially available, inexpensive ingredients such as molasses, 

brewer's yeast, cotton seed flour, or corn-steeped liquor.. Other techniques have been employed to 

improve the delivery of the biocontrol agents. A lignite-stillage (a by-product of sorghum 

fermentation) carrier system was tested for applying a T. harzianum preparation to the soil. 

Encapsulation of the biocontrol agent in an alginate-clay matrix, using Pyrax as the clay material, 

improved yield and propagule viability over time. 

Pelletized formulations of wheat bran or kaolin clay in an alginate gel containing conidia, 

chlamydospores or fermentex biomass of several Trichoderma isolates revealed increased viability 

of stored pellets, and the number of CFUs formed after adding these pellets to the soil was 

comparable to that formed from freshly prepared pellets. These growth media and delivery systems 

for formulations of biocontrol fungi show promise because they are able to introduce high levels 

(10 6- 10 10 CFU/g) of fungi into soils not steamed, fumigated, or treated with other biocides. 

To enhance biocontrol efficacy, appropriate introduction of the antagonist into the 

microenvironment appears to be crucial: formulations have been applied to seedlings prior to 

planting or to seeds in furrows. Economic considerations have forced biotechnologists to improve 

the application techniques: seed-coating, a technique involving minimal amounts of inoculum was 

developed. 

Increased biocontrol activity may be achieved by combining two types (or more, if possible) of 

biocontrol agents, for example combining Trichoderma with a bacterium, or another beneficial 

fungus. The combined activity of the antifungal compounds produced by both microorganisms 

could expand the spectrum of pathogens controlled. In fact, in field trials combining T. koningii 

with certain fluorescent pseudomonads, greater suppression of take-all disease and increased wheat 

yield were achieved relative to plants treated with T. koningii alone (Duffy et al. 1996).Delivery 

systems must ensure that biocontrol agents will grow well and achieve their purpose. It is generally 

recognized that delivery and application processes must be developed on a crop by crop and 

application by application basis. No general solutions exist, and so biocontrol systems must be 

developed for each crop. It is very important to use the organism properly and to have appropriate 

expectations. Any biocontrol organism will be unable to protect seeds as well as chemical 

fungicides. However, it colonizes roots, increases root mass and health, and consequently frequently 

provides yield increases, which chemical fungicides applied at reasonable rates cannot do. An 

effective method of use is to use the biocontrol fungus in conjunction with chemical fungicides. The 

chemicals provide good short-term seed protection, and the biocontrol fungus provides long-term 

root protection. As a consequence, yields frequently are increased over use of the chemical alone. 

Some experiences evidence that Trichoderma spp. is also highly effective when applied to 

blossoms or fruits for control of B. cinerea. Even low levels of the organism applied to strawberry 

blossoms by bee delivery or by sprays of liquid formulations are effective. For maximum control of 

the Botrytis bunch rot of grape, this initial application needs to be augmented by sprays as fruits 

mature, and addition of iprodione as a tank mix to this late application appears to have synergistic 

activity over either the biocontrol agent or the chemical fungicide alone. 

Novel applications of Trichoderma spp. Trichoderma spp. produce a variety of lytic enzymes that 

have a high diversity of structural and kinetic properties, thus increasing the probability of this 

fungus to counteract the inhibitory mechanisms used by neighbouring microorganisms. Further, 

51

Ruocco et al. 

Trichoderma hydrolytic enzymes have been demonstrated to be synergistic, showing an augmented 

antifungal activity when combined with themselves, other microbial enzymes, PR proteins of plants 

and some xenobiotic compounds (Fogliano et al. 2002; Lorito et al. 1994a, 1994b, 1994c, 1996, 

1998; Schirmbock et al. 1994; Woo et al. 2002). In fact, the inhibitory effect of chemical fungicides 

for the control of the foliar pathogen B. cinerea was substantially improved by the addition of 

minute quantities (10-20 ppm) of Trichoderma CWDEs to the treatment mixture (Lorito et al., 

1994b). 

Extensive testing of T. harzianum strain T22 conducted for the registration of this biocontrol 

agent in the USA by the Environmental Protection Agency (EPA) has found that the CWDEs do not 

have a toxic effect on humans and animals (ED50 and LD50), and that they do not leave residues, 

but degrade innocuously in the environment. Therefore, these Trichoderma hydrolytic enzymes 

present a novel product for plant disease control based on natural mycoparasitic compounds used by 

the antagonistic fungi. Single or mixed combinations of CWDEs with elevated antifungal effects, 

obtained from fermentation in inducing conditions, over-expression of the encoding genes in strains 

of Trichoderma, or heterologous expression of the encoding genes in other microbes are possible 

alternatives for pathogen control. These natural substances originating from the BCA are an 

improvement over the use of the living microorganism in the production of commercial 

formulations because they are easily characterized, resist desiccation, are stable at temperatures up 

to 60° C, and are active over a wide range of pH and temperatures in the agricultural environment. 

The important factors to consider in a commercial bio-formulation are product stability, the capacity 

to produce consistent results by preserving the characteristics producing the biological effects; the 

storability of the material, the ability to be conserved in unspecialized conditions similar to those of 

chemical pesticides; and a reasonable shelf-life or time that the product can be stored and used 

without compromising the efficacy (Agosin and Aguilera, 1998; Agosin et al., 1997; Powell and 

Jutsum, 1993). When a formulation contains the living microorganism component, the treatment 

must consist of stabilizing the viability of the BCA. For liquid formulations this can be achieved by 

maintaining the product in refrigeration (

Chapter 6 

Persistence, physiological stresses, timing and coverage of others biological agents 

Other references have been screened for biocontrol agents considering the analysis of: 

persistence on the target, 

resistance to physiological stresses, 

timing and coverage. 

Cladosporium cladosporioides. The antagonist has been effective in reducing sporulation of 

Venturia inaequalis under orchard conditions. Furthermore, the results of the pre-screening indicate 

that it is cold and drought tolerant and results of experiments on spore production in solid state 

fermentation show that mass production is economically feasible. These results have been obtained 

in a stepwise selection approach (Köhl, 2009, Köhl et al., 2009). 

Ulocladium atrum and Gliocladium roseum. Köhl et al., 1998 described the effect of treatments 

with conidial suspensions of Ulocladium atrum and Gliocladium roseum on leaf rot of cyclamen 

caused by Botrytis cinerea was investigated under commercial greenhouse conditions. Spraying U. 

atrum (1 × 106 conidia per ml) or G. roseum (2 × 106 conidia per ml and 1 × 107 conidia per ml) at 

intervals of 2 to 3 weeks during the production period and spraying U. atrum (1 × 106 conidia per 

ml) at intervals of 4 to 6 weeks resulted in a significant reduction of natural infections of petioles by 

B. cinerea. U. atrum or G. roseum (1 × 107 conidia per ml) was as effective as the standard 

fungicide program. B. cinerea colonized senesced leaves within the plant canopy and infected 

adjacent petioles and leaves later. The antagonists colonized senesced leaves and reduced B. cinerea 

development on these leaves. Thus, the inoculum potential on petioles adjacent to necrotic leaf 

tissues was reduced. The fate of U. atrum conidia on surfaces of green cyclamen leaves during a 70- 

day period after application was studied. The number of conidia per square centimetre of leaf 

surface remained relatively constant during the entire experiment. Sixty percent of the conidia 

sampled during the experiments retained the ability to germinate. When green leaves were removed 

from the plants to induce senescence and subsequently were incubated in a moist chamber, U. 

atrum colonized the dead leaves. Senesced leaves also were colonized by other naturally occurring 

fungi including B. cinerea. On leaves treated with U. atrum from all sampling dates, sporulation of 

B. cinerea was significantly less as compared with the untreated control. Our results indicate that 

early applications of U. atrum before canopy closure may be sufficient to achieve commercially 

satisfactory control of Botrytis leaf rot in cyclamen. 

Kessel et al., 2005 developed a spatially explicit model describing saprophytic colonization of 

dead cyclamen leaf tissue by the plant-pathogenic fungus Botrytis cinerea and the saprophytic 

fungal antagonist Ulocladium atrum. Both fungi explore the leaf and utilize the resources it 

provides. Leaf tissue is represented by a two-dimensional grid of square grid cells. Fungal 

competition within grid cells is modelled using Lotka-Volterra equations. Spatial expansion into 

neighbouring grid cells is assumed proportional to the mycelial density gradient between donor and 

receptor cell. Established fungal biomass is immobile. Radial growth rates of B. cinerea and U. 

atrum in dead cyclamen leaf tissue were measured to determine parameters describing the spatial 

dynamics of the fungi. At temperatures from 5 to 25°C, B. cinerea colonies expanded twice as 

rapidly as U. atrum colonies. In practical biological control, the slower colonization of space by U. 

atrum thus needs to be compensated by a sufficiently dense and even distribution of conidia on the 

leaf. Simulation results confirm the importance of spatial expansion to the outcome of the 

competitive interaction between B. cinerea and U. atrum at leaf scale. A sensitivity analysis further 

emphasized the importance of a uniform high density cover of vital U. atrum conidia on target 

leaves. 

53

Ruocco et al. 

References 

Agosin E, Volpe D, Munoz G, San Martin R, Crawford A (1997). Effect of culture conditions on 

spore shelf life of the biocontrol agent Trichoderma harzianum. World J. Microbiol. 

Biotechnol., 13:225-232. 

Agosin E, Volpe D, Munoz G, San Martin R, Crawford A (1997). Effect of culture conditions on 

spore shelf life of the biocontrol agent Trichoderma harzianum. World J. Microbiol. 

Biotechnol., 13:225-232. 

Agosin E, Aguilera JM (1998). Industrial production of active propagules of Trichoderma for 

agricultural use. In: Trichoderma and Gliocladium. Volume 2, Enzymes, Biological control 

and commercial applications, G.E. Harman and C.P. Kubicek eds., Taylor & Francis Ltd., 

London, UK, pp. 205-227. 

Ait-Lahsen, H., Soler, A., Rey, M., de La Cruz, J., Monte, E. & Llobell, A. (2001) An antifungal 

exo-alpha-1,3-glucanase (AGN13.1) from the biocontrol fungus Trichoderma harzianum. 

Appl Environ Microbiol, 67:5833-5839. 

Altomare, C., Norvell, W. A., Bjorkman, T. & Harman, G. E. (1999) Solubilization of phosphates 

and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma 

harzianum Rifai 1295-22. Appl Environ Microb, 65:2926-2933. 

Bae H, Roberts DP, Lim HS, Strem MD, Park SC, Ryu CM, Melnick RL & Bailey BA. (2011) 

Endophytic Trichoderma Isolates from tropical environments delay disease onset and induce 

resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol 

Plant-Microbe Interactions, 24:336-351 

Benitez T, Rincon AM, Limon MC & Codon AC. (2004) Biocontrol mechanisms of Trichoderma 

strains. International Microbiology, 7:249-260 

Chacon, M. R., Rodriguez-Galan, O., Benitez, T., Sousa, S., Rey, M., Llobell, A. & Delgado- 

Jarana, J. (2007) Microscopic and transcriptome analyses of early colonization of tomato 

roots by Trichoderma harzianum. Int Microbiol, 10:19-27. 

de la Cruz, J., Hidalgo-Gallego, A., Lora, J. M., Benitez, T., Pintor-Toro, J. A. & Llobell, A. (1992) 

Isolation and characterization of three chitinases from Trichoderma harzianum. Eur J 

Biochem, 206:859-867. 

de la Cruz, J., Pintor-Toro, J. A., Benitez, T. & Llobell, A. (1995a) Purification and characterization 

of an endo-beta-1,6-glucanase from Trichoderma harzianum that is related to its 

mycoparasitism. J Bacteriol, 177:1864-1871. 

de la Cruz, J., Pintor-Toro, J. A., Benitez, T., Llobell, A. & Romero, L. C. (1995b) A novel endobeta-1,3-glucanase, 

BGN13.1, involved in the mycoparasitism of Trichoderma harzianum. J 

Bacteriol, 177:6937-6945. 

Duffy, B. K., Simon, A. & Weller, D. M. (1996) Combination of Trichoderma koningii with 

fluorescent pseudomonads for control of take-all on wheat. Phytopathology, 86:188-194. 

Fogliano, V., Ballio, A., Gallo, M., Woo, S., Scala, F. & Lorito, M. (2002) Pseudomonas 

lipodepsipeptides and fungal cell wall-degrading enzymes act synergistically in biological 

control. Mol Plant Microbe Interact, 15:323-333. 

Garcia, I., Lora, J. M., de la Cruz, J., Benitez, T., Llobell, A. & Pintor-Toro, J. A. (1994) Cloning 

and characterization of a chitinase (chit42) cDNA from the mycoparasitic fungus 

Trichoderma harzianum. Curr Genet, 27:83-89. 

Hanson, L. E. & Howell, C. R. (2004) Elicitors of plant defense responses from biocontrol strains 

of Trichoderma virens. Phytopathology, 94:171-176. 

Harman, G. E. (2000) Myths and dogmas of biocontrol - Changes in perceptions derived from 

research on Trichoderma harzianum T-22. Plant Dis, 84:377-393. 

Harman, G. E. (2004) Overview of new insights into mechanisms and uses of Trichoderma based 

products. Phytopathology, 94:S138-S138. 

54

Chapter 6 

Harman, G. E. (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology, 

96:190-194. 

Harman GE. (2011) Trichoderma-not just for biocontrol anymore. Phytoparasitica, 39:103-108 

Harman, G. E., Petzoldt, R., Comis, A. & Chen, J. (2004a) Interactions between Trichoderma 

harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on 

diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology, 

94:147-153. 

Harman, G. E., Howell, C. R., Viterbo, A., Chet, I. & Lorito, M. (2004b) Trichoderma species - 

Opportunistic, avirulent plant symbionts. Nature Reviews Microbiology, 2:43-56. 

Harman, G. E., Jin, X., Stasz, T. E., Peruzzotti, G., Leopold, A. C. & Taylor, A. G. (1991) 

Production of conidial biomass of Trichoderma harzianum for biological control. Biol 

Control, 1:23-28. 

Howell, C. R. (2003) Mechanisms employed by Trichoderma species in the biological control of 

plant diseases: The history and evolution of current concepts. Plant Dis, 87:4-10. 

Howell, C. R., Hanson, L. E., Stipanovic, R. D. & Puckhaber, L. S. (2000) Induction of Terpenoid 

synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with 

Trichoderma virens. Phytopathology, 90:248-252. 

Inbar, J. & Chet, I. (1995) The role of recognition in the induction of specific chitinases during 

mycoparasitism by Trichoderma harzianum. Microbiology, 141 ( Pt 11):2823-2829. 

Jegathambigai, V., Karunaratne, M. D., Svinningen, A. & Mikunthan, G. (2008) Biocontrol of rootknot 

nematode, Meloidogyne incognita damaging queen palm, Livistona rotundifolia using 

Trichoderma species. Commun Agric Appl Biol Sci, 73:681-687. 

Jin, X., Taylor, A. G. & Harman, G. E. (1996) Development of media and automated liquid 

fermentation methods to produce desiccation-tolerant propagules of Trichoderma 

harzianum. Biol Control, 7:267-274. 

Kessel, G.J.T., J. Köhl, J.A. Powell, R. Rabinge & W. van der Werf (2005). Modelling spatial 

characteristics in the biocontrol of fungi at leaf scale: competitive substrate colonization by 

Botrytis cinerea and the saprophytic antagonist Ulocladium atrum. Phytopathology 95: 439- 

448. 

Köhl J. Screening of biocontrol agents for control of foliar diseases. In:U. Gisi et al. (eds.), Recent 

developments in management of plant diseases, Plant Pathology in the 21st Century 1, DOI 

10.1007/978-1-4020-8804-9_9, © Springer Science+Business Media B.V. 2009 

Köhl, J., M. Gerlagh, B.H. de Haas & M.C. Krijger (1998). Biological control of Botrytis cinerea in 

cyclamen with Ulocladium atrum and Gliocladium roseum under commercial growing 

conditions. Phytopathology 88, 568-575. 

Köhl, J., W.M.L. Molhoek, B.H. Groenenboom-de Haas & H.M. Goossen-van de Geijn (2009). 

Selection and orchard testing of antagonists suppressing conidia production of the apple 

scab pathogen Venturia inaequalis. European Journal of Plant Pathology 123:401-414. 

Komon-Zelazowska, M., Bissett, J., Zafari, D., Hatvani, L., Manczinger, L., Woo, S., Lorito, M., 

Kredics, L., Kubicek, C. P. & Druzhinina, I. S. (2007) Genetically closely related but 

phenotypically divergent Trichoderma species cause green mold disease in oyster 

mushroom farms worldwide. Appl Environ Microbiol, 73:7415-7426. 

Kubicek, C. P., Harman, G. E. & Ondik, K. L. Trichoderma and Gliocladium, London ; Bristol, PA, 

Taylor & Francis, 1998. 

Kubicek, C. P., Komon-Zelazowska, M. & Druzhinina, I. S. (2008) Fungal genus 

Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B, 9:753-763. 

Limon, M. C., Lora, J. M., Garcia, I., de la Cruz, J., Llobell, A., Benitez, T. & Pintor-Toro, J. A. 

(1995) Primary structure and expression pattern of the 33-kDa chitinase gene from the 

mycoparasitic fungus Trichoderma harzianum. Curr Genet, 28:478-483. 

55

Ruocco et al. 

Lora, J. M., De la Cruz, J., Llobell, A., Benitez, T. & Pintor-Toro, J. A. (1995) Molecular 

characterization and heterologous expression of an endo-beta-1,6-glucanase gene from the 

mycoparasitic fungus Trichoderma harzianum. Mol Gen Genet, 247:639-645. 

Lorito M, Woo SL, Harman GE & Monte E. (2010) Translational research on Trichoderma: from 

'Omics to the field. Annu. Rev. Phytopathology, 48:395-417 

Lorito, M., Dipietro, A., Hayes, C. K., Woo, S. L. & Harman, G. E. (1993) Antifungal, synergistic 

interaction between chitinolytic enzymes from Trichoderma harzianum and Enterobactercloacae. 

Phytopathology, 83:721-728. 

Lorito, M., Hayes, C. K., Dipietro, A., Woo, S. L. & Harman, G. E. (1994a) Purification, 

characterization, and synergistic activity of a glucan 1,3-beta-glucosidase and an N-acetylbeta-glucosaminidase 

from Trichoderma-Harzianum. Phytopathology, 84:398-405. 

Lorito, M., Farkas, V., Rebuffat, S., Bodo, B. & Kubicek, C. P. (1996) Cell wall synthesis is a 

major target of mycoparasitic antagonism by Trichoderma harzianum. J Bacteriol, 

178:6382-6385. 

Lorito, M., Broadway, R. M., Hayes, C. K., Woo, S. L., Noviello, C., Williams, D. L. & Harman, 

G. E. (1994b) Proteinase-inhibitors from plants as a novel class of fungicides. Mol Plant 

Microbe In, 7:525-527. 

Lorito, M., Hayes, C. K., Zoina, A., Scala, F., Del Sorbo, G., Woo, S. L. & Harman, G. E. (1994c) 

Potential of genes and gene products from Trichoderma sp. and Gliocladium sp. for the 

development of biological pesticides. Mol Biotechnol, 2:209-217. 

Lorito, M., Woo, S. L., Fernandez, I. G., Colucci, G., Harman, G. E., Pintor-Toro, J. A., Filippone, 

E., Muccifora, S., Lawrence, C. B., Zoina, A., Tuzun, S. & Scala, F. (1998) Genes from 

mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. P Natl 

Acad Sci USA, 95:7860-7865. 

Montero, M., Sanz, L., Rey, M., Llobell, A. & Monte, E. (2007) Cloning and characterization of 

bgn16.3, coding for a beta-1,6-glucanase expressed during Trichoderma harzianum 

mycoparasitism. J Appl Microbiol, 103:1291-1300. 

Montesinos E (2003). Development, registration and commercialization of microbial pesticides for 

plant protection. Int. Microbiol., 6: 245–252. 

Overton, B. E., Stewart, E. L. & Geiser, D. M. (2006) Taxonomy and phylogenetic relationships of 

nine species of Hypocrea with anamorphs assignable to Trichoderma section Hypocreanum. 

Stud Mycol, 56:39-65. 

Perello, A. E., Moreno, M. V., Monaco, C., Simon, M. R. & Cordo, C. (2009) Biological control of 

Septoria tritici blotch on wheat by Trichoderma spp. under field conditions in Argentina. 

Biocontrol, 54:113-122. 

Peterbauer, C. K., Lorito, M., Hayes, C. K., Harman, G. E. & Kubicek, C. P. (1996) Molecular 

cloning and expression of the nag1 gene (N-acetyl-beta-D-glucosaminidase-encoding gene) 

from Trichoderma harzianum P1. Curr Genet, 30:325-331. 

Powell KA, Jutsum AR (1993) Technical and commercial aspects of bicontrol products. J. Pestic. 

Sci., 37: 315–321. 

Samuels, G. J. (2006) Trichoderma: systematics, the sexual state, and ecology. Phytopathology, 

96:195-206. 

Samuels, G. J. & Ismaiel, A. (2009) Trichoderma evansii and T. lieckfeldtiae: two new T. hamatumlike 

species. Mycologia, 101:142-156. 

Schirmbock, M., Lorito, M., Wang, Y. L., Hayes, C. K., Arisan-Atac, I., Scala, F., Harman, G. E. & 

Kubicek, C. P. (1994) Parallel formation and synergism of hydrolytic enzymes and 

peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of 

Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol, 60:4364- 

4370. 

56

Chapter 6 

Sharon, E., Bar-Eyal, M., Chet, I., Herrera-Estrella, A., Kleifeld, O. & Spiegel, Y. (2001) Biological 

control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. 

Phytopathology, 91:687-693. 

Spiegel, Y. & Chet, I. (1998) Evaluation of Trichoderma spp. as a biocontrol agent against 

soilborne fungi and plant-parasitic nematodes in Israel. Integrated Pest Management 

Reviews, 3:169-175. 

Suarez, B., Rey, M., Castillo, P., Monte, E. & Llobell, A. (2004) Isolation and characterization of 

PRA1, a trypsin-like protease from the biocontrol agent Trichoderma harzianum CECT 

2413 displaying nematicidal activity. Appl Microbiol Biotechnol, 65:46-55. 

Tucci M, Ruocco M, De Masi L, De Palma M, Lorito M. (2011) The beneficial effect of 

Trichoderma spp. on tomato is modulated by the plant genotype. Molecular Plant Pathol. 

12:341-354 

Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Barbetti, M. J., Li, H., Woo, S. L. & 

Lorito, M. (2008a) A novel role for Trichoderma secondary metabolites in the interactions 

with plants. Physiol Mol Plant P, 72:80-86. 

Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Woo, S. L. & Lorito, M. (2008b) 

Trichoderma-plant-pathogen interactions. Soil Biol Biochem, 40:1-10. 

Viterbo, A., Haran, S., Friesem, D., Ramot, O. & Chet, I. (2001) Antifungal activity of a novel 

endochitinase gene (chit36) from Trichoderma harzianum Rifai TM. FEMS Microbiol Lett, 

200:169-174. 

Viterbo, A., Montero, M., Ramot, O., Friesem, D., Monte, E., Llobell, A. & Chet, I. (2002) 

Expression regulation of the endochitinase chit36 from Trichoderma asperellum (T. 

harzianum T-203). Curr Genet, 42:114-122. 

Woo, S., Fogliano, V., Scala, F. & Lorito, M. (2002) Synergism between fungal enzymes and 

bacterial antibiotics may enhance biocontrol. Antonie Van Leeuwenhoek, 81:353-356. 

Woo SL, Donzelli B, Scala F, Mach R, Harman GE, Kubicek CP, Del Sorbo G, Lorito M. (1999) 

Disruption of the ech42 (endochitinase-encoding) gene affects biocontrol activity in 

Trichoderma harzianum P1. Molecular Plant-Microbe Interactions, 12:419-429 

Worasatit, N., Sivasithamparam, K., Ghisalberti, E. L. & Rowland, C. (1994) Variation in pyrone 

production, lytic enzymes and control of Rhizoctonia root-rot of wheat among single-spore 

isolates of Trichoderma koningii. Mycological Research, 98:1357-1363. 

Yedidia, I., Shoresh, M., Kerem, Z., Benhamou, N., Kapulnik, Y. & Chet, I. (2003) Concomitant 

induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by 

Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl Environ 

Microbiol, 69:7343-7353. 

Yedidia, I., Srivastva, A. K., Kapulnik, Y. & Chet, I. (2001) Effect of Trichoderma harzianum on 

microelement concentrations and increased growth of cucumber plants. Plant Soil, 235:235- 

242. 

Yedidia, I. I., Benhamou, N. & Chet, I. I. (1999) Induction of defense responses in cucumber plants 

(Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ 

Microbiol, 65:1061-1070. 

57

Chapter 7 


3. Economic aspects: cost analysis 

Bernard Blum 1 , Philippe C. Nicot 2 , Jürgen Köhl 3 and Michelina Ruocco 4 

1 International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel, Switzerland 


3 Wageningen UR, Plant Research International, Droevendaalsesteeg 1, P.O. Box 69, 

6700 AB Wageningen, The Netherlands 


The industrial and commercial development of biological control agents, although needed as an 

alternative to chemical pesticides in both organic farming and IPM systems is facing different 

constraints which are particularly difficult to overcome due to the size of the involved companies 

and the early development stage of the market. These constrains can be classified within four 

categories: 

- size of the targeted market 

- cost of production 

- costs of registration 

- business profitability 

In this paper, in order to be more specific, we shall consider the situation regarding microbial 

biocontrol agents (MBCAs), using the real case of a well defined product that we cannot mention 

here due to proprietary rights. 

Size of the targeted markets 

In most of the situations MBCAs are being developed with rather small, if not niche markets. The 

total value of MBCAs sold worldwide amounted in 2008 to 620 Mio Euro (122 Mio Euro in 

Europe) including products with insecticidal or fungicidal effects. This value can be compared with 

the sales of chemical insecticides and fungicides amounting to a total of 21 000 Mio Euros. 

MBCAs, with the exception of Bt products which can be used in larger crops such as grapes, 

forestry or even cereals, are presently still used in speciality crops, greenhouses and covered crops. 

The size of these crops is not growing anymore or at a very reduced rate. The only optimistic 

perspective is the intention to develop organic faster farming (objective 20% of the production area 

in France in 2030) where MBCAs can find a good market. 

Additionally the potential market is widely fragmented within a long list of crops such as 

carrots, petersillium, onions, etc, usually referred to as “Minor crops”. These markets are so small 

that even large chemical companies refrain from the investments that would cover the needs and the 

manufacturers of MBCAs, due to the specificity of their products, are obliged to invest and cover 

costs where scale economy can never be reached. 

Cost of production 

Contrary to the synthesis of chemicals, producing MBCAs requires a complicated and extremely 

expensive process of production which can be divided into four phases: fermentation, extraction, 

58

Chapter 7 

purification, formulation and packaging. All these phases are difficult and require relatively heavy 

costs. 

Fermentation. This first step has to be undertaken either with solid or with liquid phase 

technology. Although the liquid phase fermentation is usually simple and cost effective, the process 

is more risky because the produced spores are more fragile. In the contrary using solid fermentation 

substrates will produce stronger, but it becomes more difficult to increase the production volume. 

Extraction. Here again, there is a very strong difference between the MBCAs produced in 

liquid or in solid fermenters. In a liquid, the extraction will be rather easy by filtration, but the 

product will need to be dried, which is a very long, energy-demanding and expensive process. From 

a solid fermentation process, the extraction will be mechanical. Such a process is rather harmful for 

the spores: It is again energy demanding and it is extremely difficult to extract more that 60% of the 

spores from a substrate. In such a case the productivity becomes rather poor. 

Purification. This step is very important to ensure the stability of the MBCAs produced. The 

industrially produced MBCAs always contain impurities which, although biologically inactive, may 

become critical over time, potentially creating risks of degradation, inactivation etc. In all situations 

the purification step requires a high level of sophistication and expensive processes. 

Formulation and packaging. Formulation and packaging of MBCAs, due to their living state 

(and the requirement that they remain alive for satisfactory effectiveness of the product), constitute 

an extremely difficult step and in any case more expensive than the equivalent process for 

chemicals. The choice of co-formulants, adjuvants and packaging material must secure the quality 

of the MBCAs and its vitality. This is again a source of problems and heavy costs. 

Additionally to all the above mentioned hurtles, it has to be secured that no contamination will 

occur, during the fermentation process naturally, but also during the extraction, the purification, the 

formulation and the packaging. All the safety measures are very expensive to carry out, but they are 

necessary in order to ensure the quality of the product brought to the market. As a consequence of 

all these extra expenses and technical difficulties the MBCAs used for this analysis were more than 

2.5 times more expensive to produce than an equivalent chemical pesticide (Table 14). 

Table 14: Compared structure of the production costs for a microbial biocontrol agent (MBCA) 

and a chemical insecticide (source IBMA). 

Typical Insecticide MBCA Comments 

Sales value 100 100 

Type of production cost 

Raw materials %* 8 29 40% lost material for 

MBCA by solid 

fermentation process 

Packaging 1 2 

Energy and miscellaneous 1 2 

Manpower 5 9 

Consumables 2 3 

Amortisation 4 11 

TOTAL 21 56 

* costs are expressed as percent of the sales value of the commercial product 

Cost of registration 

It has been already mentioned that biological control agents suffer from a highly unfavourable 

situation compared to chemical pesticides. The regulations for registration have initially been set up 

to reduce the risks attached to molecules and the regulator is trying to extrapolate these 

requirements for the registration of living organisms. 

59

Blum et al. 

The estimated cost for registering a microbial biocontrol agent is currently lower than that for a 

chemical pesticide (Table 15). However, the size of this investment is still very high for a company 

in comparison with the market potential (Table 16).This evaluation indicates that the introduction 

on the market of a MBCA is about 4 times less effective than its chemical equivalent. 

Table 15: Compared potential costs of registration for a microbial biocontrol agent (MBCA) and a 

chemical pesticide (source IBMA) 

Area 

Toxicity of the 

active substance 

Study Type 

Cost for Cost for 

Chemical (€) MBCA (€) 

Acute studies (6 tests) 140 000 140 000 

Sub-acute (rat study) 140 000 120 000 

Mutagenicity 40 000 may be waived 

Toxicity on cultured cells 10 000 not required 

Acute studies 140 000 140 000 

Toxicity of the 

formulation Toxicity on cultured cells 10 000 not required 

Environmental 

fate 

Soil, water, air 200 000 70 000 

Biology Mode of action etc 150 000 *50 000 

Ecotoxicology of Birds, fish, bees, algae, daphnia, earthworm 60 000 40 000 

active substance Beneficials 20 000 may be waived 

Ecotoxicology of Birds, fish, bees, algae,daphnia, earthworm 60 000 40 000 

formulation Beneficials 20 000 

Residues 

8 trials / crop 80 000 may be waived 

Development of analytical methods 100 000 **variable 

Formulation Physical properties, shelf life, etc. 200 000 220 000 

Efficacy 8 field trials 40 000 40 000 

TOTAL 1 410 000 860 000 

* cost of strain identification 

** e.g. development of strain-specific markers 

Table 16: Compared estimated market potential for a microbial biocontrol agent (MBCA) and for a 

chemical pesticide (source: IBMA) 

Year 

Estimated sales value ( Mio€) 

Chemical pesticide 

MBCA 

1 0.1 0.05 

2 1.2 0.15 

3 6.0 0.90 

4 15.0 1.50 

5 35.0 3.50 

Total early sales 57.3 6.10 

Plateau sales 120.0 15.00 

Registration costs 1.410 0.860 

Ratio registration/ early 

sales 

Ratio registration/ 

Plateau sales 

2.4 % 14.0 % 

1.1 % 5.7 % 

60

Chapter 7 

Business profitability 

Comparing estimated production and other costs, relative to the sales value at plateau level, points 

out large differences between chemical pesticides and microbial biocontrol agents (Table 17). The 

gap between the two in terms of estimated profit is nearly 10-fold in favour of the chemical 

industry. 

Table 17: Compared margin structure estimates for the production and sales of a microbial 

biocontrol agent (MBCA) and a chemical pesticide (source IBMA) 

%* Chemical pesticide MBCA 

Sales value at plateau level 100 100 

Costs of production 21 56 

Gross margin 79 44 

Cost of sales 21 15 

Cost of research 8 12 

Cost of administration 4 3 

Earnings before investments taxes 

46 14 

and amortisation (EBITA) 

Profit after taxes, provisions and 

18 2 

amortisation 

* costs and margins are expressed as percent of the sales value of the commercial product 

Conclusion and outlook for industry 

These data show clearly that the profitability of a biocontrol business is much less attractive than 

that of chemical pesticides and may explain why the large chemical companies decided in the 90’s 

to retreat from this business. Although these companies show presently some new signs of interest, 

they seem to remain basically reluctant to re-enter despite the new attractiveness of a fast growing 

biocontrol market. Contrary to European and US-based companies, several Japanese firms, such as 

Sumitomo chemicals or Mitsui appear to have invested for a potential long term return. Taking 

advantage of the divestment by the chemical majors, they have been able to acquire a good business 

basis at very attractive conditions. This should enable them to consider optimistically the future 

development of the biocontrol industry and its positive trend. 

The smaller companies which have invested in this business and try to overcome their financial 

problems have only two alternatives: 

- Either develop, often at a loss, into larger markets (grapevine, field crops etc), if they can. In 

order to sustain these efforts, they will need a strong support from venture capital 

companies; 

- or enter into venture agreements with other manufacturers/suppliers, in order to build up a 

product portfolio which will make them successful in the future. 

61

Chapter 8 


4. Socio-economic aspects: market analysis and outlook 

Bernard Blum 1 , Philippe C. Nicot 2 , Jürgen Köhl 3 and Michelina Ruocco 4 






With estimated sales amounting to only 200 Mio€ in Europe in 2008, the market for biological 

control agents appears to be extremely small compared with the 7 000 Mio€ turnover achieved with 

chemical pesticides. However, very important efforts have been undertaken for the development of 

biocontrol agents. The OECD estimated that 5 000 Mio$ have been spent worldwide in public 

research for biocontrol during the last 40 years. This amounts to a yearly average of 500Mio$, not 

far from the 600 Mio$ spent yearly in research by the agrochemical industry, but with a 

comparatively poor result! 

In the Conference on biological control organised in 2003 by IBMA in Béziers, France, the 

major stakeholders (farmers, retailers, distributors, regulators etc.) have provided a list of gaps 

considered to play a role in preventing wide adoption of biocontrol products. This list was meant to 

cover all potential explanations, but provided neither figures nor priority ranking, making it difficult 

to prioritize actions for improvement. It was however a general opinion that the complicated and 

costly system of registration was the major reason of the problem. As a result, important efforts 

have been undertaken to convince the regulators to adopt more facilitating procedures for the 

registration of biologicals. These efforts were not without effect and the newly adopted “Pesticides 

package” makes it easier, under certain conditions, to register biologicals. In the meantime, several 

EU member states have adopted easier registrations tracks, such as the Biopesticides Scheme in the 

UK, for example. 

In reality, the unique assumption that the current regulations in Europe significantly hamper 

the development and the use of biologicals does not seem to be proven by the facts. During a very 

long period, the biologicals were not subject to registration and very few products were brought 

successfully to the market. At the same time countries such as the USA, New Zealand or Japan have 

adopted very liberal registration procedures, but the sales of biologicals remain marginal. 

In the frame of ENDURE, it has been therefore decided to get a detailed and quantified idea on 

the gaps which, in Europe, restrain the adoption of biologicals, especially at the users and 

commercial levels. In order to achieve this objective, a Pan-Europa survey was undertaken from 

2007 until 2008, with the assistance of the public opinion organisation Agridata. 

Methodological approach: survey of European farmers 

Since no validated data were available about the real market and the use of biological control agents 

in Europe, it has been necessary to build up a form of electronic map of the European agriculture 

and of the distribution of the potential users. 

62

Chapter 8 

A survey was carried out to evaluate the size of the biocontrol market in Europe and to identify key 

factors that could influence its future evolution. This study included four main steps: 

- Localisation of the main crops and cropping systems. 

Using the data from EUROSTAT and national statistics a model of European agriculture was 

constructed. 

- Randomised sampling of farmers and retailers. 

The model was used for the selection of 12 production systems (Table 18) located on 25 sites in 

9 countries (Table 19) where 2000 farmers and 21 retailers were identified. 

- The selected sample was contacted by phone directly and a questionnaire (Table 20) was sent to 

those who agreed to participate in the survey. A total of 675 full responses were obtained and 

analysed. 

- Complementary survey. 

In order to validate the process, more specific data was collected in a survey concerning the 

biological control of wood diseases of grapevine in France 

Table 18: Production systems selected for a survey of factors influencing biocontrol use in Europe 

(source IBMA) 

Type of cropping system 

Large arable crops 

Multicropping 

arable crops dominant 

animal production dominant 

Fruit production 

orchards 

grapes 

Tomato production 

protected 

field 

Geographical sub-categories 

North, South 

Mountains, North, South 

Mountains, North South 

Table 19: Geographical distribution of sampling sites for a survey of factors influencing biocontrol 

use in Europe (source IBMA) 

Country 

number of 

sampling site 

Austria 2 

Denmark 1 

Germany 4 

Greece 2 

France 4 

Italy 4 

Poland 3 

Spain 3 

United Kingdom 2 

63

Blum et al. 

Table 20: Structure of the questionnaire used in a survey of European farmers and retailers of 

biological control products 

Categories of questions 

Nbr of Questions 

Geographical identification 5 

System of production concerned 12 

Ownership and social related aspects 5 

Crop protection issues / pest occurrence, etc 18 

Economy of the farm, actual costs, revenues etc 12 

Expectations for future, cropping systems, investments, etc 9 

Relations with input suppliers 18 

Relations with advisors 18 

Relations with authorities 18 

Relation with the food chain (coops, supermarkets etc.) 18 

Relations with the consumers 18 

Relations with the public 18 

Expectations about innovations, role of science 12 

Open comments 2 

Survey Results: The estimated market of biocontrol in Europe 

The questionnaire made it possible to estimate the total biological market in ha and in value (Figure 

11) and its partition among different crops (Figure 12). 

These data confirm that in 2008, the main use of biologicals was in protected crops, followed 

by grapevine and fruit production. Nearly 40% of the estimated biocontrol market consisted in sales 

of beneficial insects, compared to 25% for microorganisms and 21% for semiochemicals (Figure 

11). 

Total estimated EU sales of biocontrol products = 204 Mio€ in 2008 

18 Mio€ 

43 Mio€ 

52 Moi€ 12 Mio€ 

79 Mio€ 

Beneficial insects 

Beneficial nematods 

Microbial biocontrol agents 

Semiochemicals 

Natural substances 

Figure 11: Estimated sales of biocontrol products in Europe in 2008 (in Million €). The estimates 

were obtained by extrapolating use patterns in a representative sample of EU farmers. 

64

Chapter 8 

80 

70 

60 

%of supply 

%of acreage 

% of total 

50 

40 

30 

20 

10 

0 

Protected crops 

Field vegetables 

Grapes 

Fruits 

Field crops 

Gardens, ornamentals 

Figure 12: Estimated distribution of biocontrol use among types of crops in 2008 in Europe 

Survey results: Factors of development of biocontrol 

The exploitation of the questionnaires was somewhat difficult due to the large variety of farmers 

and situations. Additionally, several open ended questions were introduced to collect opinions on 

possible additional gaps and opportunities which were not mentioned in the form. 

Qualitative analysis. In a first step, the analysis of the responses led to the identification of 12 

factors deemed to have a significant influence on the future development of biological control 

Nine factors with a positive influence: 

o Ability of manufacturers to invest in R&D 

o Financial strength of manufacturers 

o Direct involvement of leading distributors 

o Pull from the fresh food wholesalers and from the food industry 

o Demand from consumers and NGOs 

o Incentives given to growers 

o Education of advisors and growers 

o Availability of Decision Support Systems (DSS) 

o Regulatory obstacles to chemical pesticides 

Three factors with a negative influence: 

o Regulations not adapted to Biological control 

o Discovery of novel effective and safe chemicals 

o Development of new resistant crops 

Quantitative analysis. In a second step, a quantitative analysis was conducted to estimate the 

influence of the identified factors. For this, 320 contacts (50% of the sample) were requested to 

65

Blum et al. 

indicate which of the 12 factors they considered as important in terms of their potential impact on 

the evolution of future use of biological control agents. For those factors selected as important, the 

respondents were asked to weigh the expected impact positively or negatively on a scale from 0 to 

20. 

The data were used to compute for each of the 12 factors: 

a) an Influence Index, calculated as the percentage of respondents who selected the factor as 

important 

b) a Weight Index, calculated as the average of the weights attributed to the factor by those 

respondents who selected it as important 

c) a Growth Index, combining the two other indices according to the following formula: 

GI = (Influence Index)*(Weight Index)/10 

This index represents the overall estimate of the influence of a factor on the future use of 

biological control agents by European farmers. 

The scores computed for each of the 12 factors are presented in Table 21. Among the factors 

deemed to carry the most impact on future use of biological control by European farmers the action 

by far the most cited was the establishment of incentives for farmers (factor D). 

Table 21: Impact of twelve factors on the future use of biocontrol agents by European farmers 

according to a survey of 320 farmers 

A 

Factors 

Registration for biological control 

products remains as present 

Influence 

Index (%)* 

Weight Index* 

(scale from 

-20 to +20) 

Growth 

Index* 

12 - 15 - 18.0 

Rank of 

positive 

influence 

B Involvement of distribution 65 8 52.0 4 

C Size / strength of the manufacturers 55 12 66.0 3 

D Incentives to growers 87 18 156.6 1 

E Education of advisors and growers 27 8 21.6 5 

F Decision Support Systems available 12 7 7.2 9 

G 

Pull from wholesalers and food 

industry 

43 16 66.8 2 

H Stringent registration of chemicals 16 14 22.4 6 

I New safe chemical pesticides 42 - 12 - 3.0 

J Progress in R&D of Biocontrol 8 14 11.2 8 

K New resistant varieties 16 - 4 - 6.4 

L Pull from Consumers 67 2 13,4 7 

* see main text above for the specific definition of the indices 

The second most important factors based on the Growth Index (G, C and B in Table 21) were 

linked to the influence of key economic actors (the wholesalers, the food industry, the distributors 

and manufacturers of biocontrol products). The factors with the lowest scores were those related to 

scientific innovation (factors K, I, J). Interestingly, both factors linked to regulatory aspects (factors 

H and A) also had a relatively low Growth Index. The registration requirements are obviously more 

a concern for the industry than for the users of the plant protection products. Surprisingly, the 

66

Chapter 8 

efficacy and the price of the biologicals, usually considered as two critical factors, were not 

mentioned as real constraints. This may be due to two reasons: 

(1) It is anticipated that only “effective” solutions will be registered in the EU, showing the high 

confidence of the farmers and the retailers in the registration systems 

(2) The selling price of the new solutions (biological control products) will necessarily cope with 

the current price levels. Too highly priced, the new solutions will simply be ignored. 

Conclusions 

The gaps and the opportunities for the development of biological crop protection products are 

extremely relative to people concerned. While the industry, due to the heavy factor time/cost to the 

market, considers the regulation requirements as a major obstacle, the users and the retailers are 

much more influenced by the pull and push actions exercised at the market level. Somewhat 

disappointing is the relative low concern about the technical progress offered by the biological 

solutions. 

67


Perspectives for future research-and-development projects on biological 

control of plant pests and diseases 

Philippe C. Nicot 1 , Bernard Blum 2 , Jürgen Köhl 3 and Michelina Ruocco 4 






The review of published scientific literature on the biological control of selected pests and diseases 

has lead to the identification of clear knowledge gaps highlighted in previous chapters. Further 

bottlenecks were revealed by seeking the possible reasons for the striking discrepancy between the 

rich inventory of potential biocontrol agents described by scientists and a very small number of 

commercial products on the market. 

To complement these analyses, the participants of Research Activity 4.3 of the European 

Network ENDURE organized consultations of experts (scientists, extension specialists and 

representatives of the Biocontrol industry) at the occasion of scientific meetings of three Working 

Groups of IOBC-wprs. 

- Working Group "Integrated Control of Plant Pathogens": meeting on "Molecular Tools for 

Understanding and Improving Biocontrol" in Interlaken (Switzerland) September 9-12, 2008. 

(attended by P.C. Nicot and B. Blum – discussion session about the outlook on biocontrol 

against plant diseases) 

- Working Group “Multitrophic Interactions in Soil” meeting in Uppsala (Sweden), 10-13 June 

2009. (attended by C. Alabouvette – roundtable about the outlook on biocontrol of soilborne 

pests and diseases) 

- Working Group "Insect Pathogens and Insect Parasitic Nematodes": meeting on "Future 

Research and Development in the Use of Microbial Agents and Nematodes for Biological Insect 

Control" in Pamplona (Spain), 22-25 June, 2009 (attended by C. Alabouvette – his plenary 

presentations about the outlook on biocontrol of diseases and pests has been published * ). 

These consultations were further complemented by discussions at the occasion of various 

meetings of participants of Research Activity 4.3 to identify the most prominent issues that could be 

tackled by future research and development activities. The key elements are organised below in 

three categories, based on their relevance to the concern of the research community, development or 

industry. 

Research issues 

Five key issues have been identified in term of research needs: 

Devise better strategies for the screening of biocontrol agents. The demand for new 

biocontrol agents is already high. It is expected to increase sharply in the EU, with the ongoing 

* Alabouvette, C, Cordier, C. 2009 Biological control of plant diseases: Future research goals to make it successful. 

IOBC/WPRS Bulletin 45:3-5. 

68


reduction of available chemical pesticides and the need for new non-chemical plant protection tools 

to comply with Directive 2009/128/EC. Current methods need to be improved both in terms of 

logistics (high throughput to allow rapid mass screening of large numbers of candidates) and in 

terms of the pertinence of criteria for efficacy, production and commercialization. This topic has 

been tackled within Research Activity 4.3 of the European Network ENDURE for microbial 

biocontrol agents against diseases (Deliverable DR4.9) and the results have been published (Köhl et 

al., 2011 * ). 

Improve knowledge on efficacy-related issues. The criteria traditionally used to asses the 

efficacy of biological control methods may be misleading because contrarily to conventional 

pesticides, biocontrol does not intend to eradicate pests and diseases but, rather, to install a 

biological balance which will enable the plants to grow more healthily. However the consistency of 

field efficacy remains one of the constraints for the large scale use of biological control of plant 

diseases. Despite much recent progress, research efforts are still necessary for (1) a better 

understanding of key parameters of field efficacy in relation to the type of biocontrol agent and their 

modes of action and (2) implementing the most promising methods for efficacy improvement. 

Promising avenues of research are to be sought both in terms of exploiting the biological properties 

of the biocontrol agents and enhancing their effectiveness through formulation of the products. 

Results obtained on these topics should provide key information both for the design of optimised 

production and application strategies, but also for improving the screening process of future 

biocontrol agents as mentioned in the point above. 

Promote multidisciplinary approaches to integrate better biocontrol with IPM and other 

production issues. Based on passed published experience, it is clear that levels of protection 

provided by a single biocontrol agent alone will seldom be sufficient, especially when faced with 

field conditions unfavourable to their effectiveness or with very high inoculum pressures of a pest 

or plant pathogen. More emphasis will need to be placed on the compatibility of biocontrol agents 

with the implementation of IPM, preferably in a systemic approach of integrated production. 

Among the many possible interactions to be considered, compatibility and combined used of 

biocontrol and plants genetically modified for improved resistance to pest or plant diseases should 

not be overlooked. 

Develop adapted delivery technologies. Much progress has been made in packaging 

technology and delivery for macrobial biocontrol agents (e.g. beneficial arthropods). In contrast, 

treatments with microbial biocontrol agents (against pests or diseases) still rely on sprayers 

developed for the application of pesticides. Research is needed to provide growers with low 

pressure spraying equipment to preserve the viability of the microbials. Technological 

improvements are also needed for optimal coverage of the target plant surfaces to be protected by 

the biocontrol agents. 

Safeguard the durability of biocontrol. Certain pests and pathogens are known for their 

capacity to develop resistance to chemical pesticides or to overcome varietal resistance. The 

durability of biological control has often been assumed to be higher than that of chemical control, 

but several examples of resistance of pests have already been reported. Much less is known about 

plant pathogens, probably in part because biological control against diseases is still very rare. 

Significant research efforts are needed to anticipate the potential hurtles in this domain and integrate 

durability concerns both in the screening of new biocontrol agents and in the careful management of 

their use once they become commercially available. 

* Köhl, J., Postma, J., Nicot, P., Ruocco, M., Blum, B. 2011. Stepwise screening of microorganisms for commercial use 

in biological control of plant pathogenic fungi and bacteria. Biological Control 57, 1-12. 

69

Nicot et al. 

Issues for development 

Three key issues have been identified in terms of development. They are directly related to 

improving the efficacy of crop protection but also to acceptability of biocontrol by farmers. 

Training of advisers and farmers. Compared to chemical control, the implementation of 

biological control presents an additional level of technical complexity when the "active substance" 

is a living organism or microorganism, whose liveliness and development on the target crop 

underpins the effectiveness of the protection. In many situations, achievement of successful 

biocontrol of pests has been linked to an active role of advisers in accompanying the farmers, at 

least during their initial phase of adoption and implementation. The success of large scale use of 

biological control in the future will require stepping up the technical training of farmers and of 

advisors. Such action will also positively influence the adoption issues mentioned below. 

Development and dissemination of Decision Support Systems (DSS). Growers routinely 

make decisions that take into account multiple constraints (both technical and economic) of their 

activity. However, the complexity of biocontrol and its necessary integration in a systems approach 

of crop protection and crop production make DSS more and more indispensible, including in their 

function as easily consultable repositories of knowledge on available choices. 

Establishment of demonstration schemes and development of farmers' networks. This 

action is needed to stimulate the dissemination of information to and among farmers, but also to 

facilitate exchange between the end users of biocontrol and the other actors of research, 

development and commercialization of the products. Breaking up regional and national barriers and 

including a European dimension to such networks is desirable for optimal efficacy of multisite 

experimental trials. 

Industrial issues 

Quality control. Ongoing efforts by the manufacturers of biological control agents to 

guarantee the quality of their products need to be stepped up. The definition of tests and their 

routine implementation is crucial to ensure reliable effectiveness and maintain confidence of 

farmers for biocontrol. Whenever possible, such tests should include not only an evaluation of 

viability of the biocontrol agent but also an evaluation of physiological parameters related to its 

efficacy, based on knowledge of its modes of action. 

Improve distribution systems. Distibution systems need to be improved to safeguard the 

quality of the products and provide technical advice for the users. In many cases, the distribution of 

biocontrol products is common with that of chemical pesticides. One possible avenue of progress 

would be to improve awareness on the specificities of handling biocontrol products, especially those 

containing living organisms or micro-organisms. Another would be the development of sizeable 

distributions networks focused on biocontrol, which could be brought together by groups of 

(currently often small) producers of biocontrol products. 

70

Appendices 

For Chapter 1 

Appendix 1. 

Appendix 2. 

Appendix 3. 

Appendix 4. 

Appendix 5. 

Appendix 6. 

Inventory of biocontrol agents described in primary literature (1998-2008) for 

successful effect against Botrytis sp. in laboratory experiments and field trials 

with selected crops 


successful effect against powdery mildew in laboratory experiments and field 

trials on selected crops. 


successful effect against the rust pathogens in laboratory experiments and field 

trials on selected crops 


successful effect against the downy mildew / late blight pathogens in laboratory 

experiments and field trials on selected crops 


successful effect against Monilinia in laboratory experiments and field trials on 

selected crops 

Primary literature (2007-2009) on biological control against Fusarium oxysporum 

For Chapter 2 

Appendix 7. 

Appendix 8. 

Number of references retrieved by using the CAB Abstracts database in order to 

review scientific literatures on augmentative biological control in selected crops 

for Chapter 2. 

Collection of data on augmentative biological control of pests in grapevine. Each 

table refers to a group of biocontrol agents. 

For Chapter 3 

Appendix 9. References on classical biological control against insect pests (cited in Chapter 3) 

For Chapter 4 

Appendix 10. Substances included in the "EU Pesticides Database" as of April 21 2009 

Appendix 11. Invertebrate beneficials available as biological control agents against invertebrate 

pests in five European countries. 

71

Appendix 1. Inventory of biocontrol agents (M: microbials; B: botanicals; O: others) described in primary literature (1998-2008) for 

successful effect against Botrytis sp. in laboratory experiments and field trials with selected crops 

Tomato + Cucumber + Pepper (target pathogen = B. cinerea) 

Success in field trials 

Success in laboratory conditions (in vitro and/or in planta in controlled conditions) 

M 

Bacteria 

Bacillus amyloliquefaciens BL3, pepper (Park et al., 1999) 

Bacillus licheniformis > FG (Lee et al., 2006) 

Bacillus subtilis strain QST 713 (Serenade ASO) (Ingram and Meister, 2006), 

Quadra 136, preventive (Utkhede and Mathur, 2006) 

Brevibacillus brevis (Seddon et al., 2000) (McHugh et al., 2002) (Schmitt et al., 

2001) 

Brevibacillus brevis WT + Milsana / cucumber (Konstantinidou-Doltsinis et al., 

2002) 

Paenibacillus polymyxa BL4, pepper (Park et al., 1999) 

Pseudomonas putida Cha94, pepper (Park et al., 1999) 

Streptomyces (Mycostop(R), (Lahdenpera and Korteniemi, 2008)actinomyces 

(Yao et al., 2007), strains III-61 and A-21 (Pan et al., 2005) 

Bakflor (consortium of valuable bacterial physiological groups) (Kornilov et al., 

2007) 

Fungi + yeasts: 

Clonostachys rosea (ADJ 710 OMRI), (Shipp et al., 2008) 

Gliocladium sp. (Georgieva, 2004) 

Gliocladium catenulatum Prestop(R), preventive (Utkhede and Mathur, 2006) 

(Utkhede and Mathur, 2002) (Lahdenpera and Korteniemi, 2008) 

Gliocladium viride (Lisboa et al., 2007) 

Microdochium dimerum (Nicot et al., 2003) (Trottin-Caudal et al., 2001) 

Rhodosporidium diobovatum S33 preventive (Utkhede and Mathur, 2006) 

curative (Utkhede and Mathur, 2002), /cucumber (Utkhede and Bogdanoff, 

2003) 

Trichoderma sp. (Georgieva, 2004) 

Trichoderma harzianum (Lisboa et al., 2007), T39 (Trichodex) tomato (Apablaza 

and Jalil R, 1998) (Moreno Velandia et al., 2007), tomato + cucumber 

(Elad, 2000b) (Dik and Wubben, 2001) / cucumber (Elad, 2000a), TM / 

pepper (Park et al., 1999), RootShield curative (Utkhede and Mathur, 2002), 

T22 PlantShield(R) curative (Utkhede and Mathur, 2006) 

Variable little or no effect once in the field (good in lab): 

Brevibacillus brevis WT / cucumber (Konstantinidou-Doltsinis et al., 2002) 

Gliocladium catenulatum (Prestop). (Ingram and Meister, 2006) 

Trichoderma (tomato + pepper) (Salas Brenes and Sanchez Garita, 2006) 

Trichoderma harzianum T39 Trichodex with BOTMAN (Moyano et al., 2003) 

Bacteria 

Bacillus antagonists (Tsomlexoglou et al., 2000) (Enya et al., 2007) (Tsomlexoglou et al., 2001) (Tsomlexoglou et 

al., 2002) 

Bacillus circulans (Wang et al., 2008b) 

Bacillus subtilis (Wang et al., 2008b) (Sadfi-Zouaoui et al., 2007a) (Gu et al., 2008) (Sadfi-Zouaoui et al., 2007b) 

Bacillus licheniformis (Lee et al., 2006) (Sadfi-Zouaoui et al., 2007a) 

Brevibacillus brevis (White et al., 2001) (Seddon and Schmitt, 1999) (Seddon et al., 2000) (Allan et al., 2003) 

Cupriavidus campinensis / cuc, tom (Schoonbeek et al., 2007) 

Halomonas subglaciescola, Halobacillus litoralis, Marinococcus halophilus, Salinococcus roseus, Halovibrio 

variabilis, Halobacillus halophilus, Halobacillus trueperi (Sadfi-Zouaoui et al., 2008) 

Halomonas sp. K2-5 (Sadfi-Zouaoui et al., 2007b) 

Micromonospora coerulea (Kim et al., 1999) 

Pantoea (Enya et al., 2007) 

Pseudomonas aeruginosa (Hernandez-Rodriguez et al., 2004) 7NSK2 (Audenaert et al., 2002) 

Pseudomonas fluorescens (Yildiz et al., 2007) (Hernandez-Rodriguez et al., 2004) 

Burkholderia cepacia (Hernandez-Rodriguez et al., 2004) 

Serratia plymuthica HRO-C48 (Ma et al., 2007), IC1270 (Meziane et al., 2006), IC14 / cucumber (Kamensky et 

al., 2002, Kamensky et al., 2003) 

Streptomyces ahygroscopicus var. wuyiensis (Sun et al., 2004) 

Streptomyces lydicus/ cucumber (Farrag, 2003) 


Aureobasidium pullulans (Dik et al., 1999) (Dik and Elad, 1999) 

Beauveria sp. (Diaz et al., 2007) 

Candida guilliermondii strains 101 and US 7 (Saligkarias et al., 2002) 

Candida oleophila strain I-182 (Saligkarias et al., 2002) 

Candida pelliculosa (Bello et al., 2008) 

Clonostachys rosea (Nobre et al., 2005) (Sutton et al., 2002) (Yohalem, 2001) 

Cryptococcus laurentii (Xi and Tian, 2005) 

Cryptococcus albidus (Dik et al., 1999) (Dik and Elad, 1999) 

Gliocladium (Hmouni et al., 2005) (Hmouni et al., 2006, Hmouni et al., 1999) 

Gliocadium viride (Bocchese et al., 2007) (Lisboa et al., 2007) 

Microdochium dimerum (Bardin et al., 2008) (Bardin et al., 2004b) (Bardin et al., 2004a) (Decognet and Nicot, 

1999) (Decognet et al., 1999) (Trottin-Caudal et al., 2001) (Nicot et al., 2002) 

Pichia guilliermondii (Zhao et al., 2008) 

Rhodosporidium diobovatum (S33), (Utkhede et al., 2001) 

Rhodotorula glutinis Y-44 (Kalogiannis et al., 2006) 

Rhodotorula rubra (Bello et al., 2008) 

Trichoderma (Hmouni et al., 2005) (Hmouni et al., 1999) 

Trichoderma harzianum (Hmouni et al., 2006) (Fiume et al., 2008) (Barakat and Al-Masri, 2005) (Lisboa et al., 

72

Appendix 1 

B 

O 

Milsana + Brevibacillus brevis WT / cucumber (Konstantinidou-Doltsinis et al., 

2002) 

Variable little or no effect once in the field: 

Reynoutria sachalinensis extract (Milsana); (Ingram and Meister, 2006) 

calcium foliar fertilizers (CaH2O2, CaSO4, Ca(NO3)2, CaCl2 and CaO), 

(Mizrakci and Yildiz, 2002) 

2007) T115 (Meyer et al., 2001) Trichodex T39 (Elad et al., 1998) (Yohalem et al., 1998) (Meyer et al., 1998) 

(Jalil R et al., 1997) (Dik et al., 1999) (Dik and Elad, 1999), RootShield (Utkhede et al., 2001), Th-B /pepper 

(Li et al., 2004), Rifai (Gromovikh et al., 1998) 

Trichoderma taxi ZJUF0986 (Wang et al., 2008a) 

Trichosporon pullulans (Cook, 2002) 

Ulocladium atrum (Nicot et al., 2002) (Fruit and Nicot, 1999) (Yohalem, 2001) / cucumber (Yohalem, 1997) 

Ustilago maydis (Teichmann et al., 2007) 

Oomycetes 

Pythium oligandrum (Floch et al., 2001) (Wang et al., 2007a) 

Little or no effect once in the field (good in lab): 

Trichoderma spp. commercial preparations/ cucumber (Yohalem, 1997) 

volatile substances produced by grape cv. Isabella (Vitis labrusca) (postharvest) (Kulakiotu et al., 2004) (Kulakiotu 

and Sfakiotakis, 2003) 

Compost water extracts prepared from animal sources (horse, sheep, and cattle) and a plant source (olive), 

(Hmouni et al., 2006) 

Adipic acid monoethyl ester (Vicedo et al., 2005) 

Calcium foliar fertilizers (CaH2O2, CaSO4, Ca(NO3)2, CaCl2 and CaO), (Mizrakci and Yildiz, 2002) 

Chitosan Elexa (Acar et al., 2008) 

Benzothiadiazole (BTH) (Hernandez-Rodriguez et al., 2004) 

Variable little or no effect : 

Vital pasta, Vital gel and Elot-Vis (Gielen et al., 2004) 

73

Nicot et al. (Appendix for Chapter 1) 

Grapes (target pathogen = B. cinerea) 


M 

Bacteria 

Acinetobacter lwoffii PTA-113, (Magnin-Robert et al., 2007) 

Pseudomonas fluorescens PTA-CT2, (Magnin-Robert et al., 2007) 

Pantoea agglomerans PTA-AF1 (Magnin-Robert et al., 2007) 

Bacillus (isolate UYBC38) (Rabosto et al., 2006) 

Bacillus subtilis strain QST 713 (serenade) (Benuzzi et al., 2006) Serenade, 

moderate to good control (Schilder et al., 2002) 


Acremonium cephalosporium, strain B11 (Zahavi et al., 2000) 

Candida guilliermondii, strain A42 (Zahavi et al., 2000) 

Chaetomium cochlioides (Lennartz et al., 1998) 

Gliocladium (Cherif and Boubaker, 1998) 

Gliocladium roseum (Holz and Volkmann, 2002) 

Hanseniaspora uvarum (isolate UYNS13) (Rabosto et al., 2006) 

Trichoderma (Cherif and Boubaker, 1998) 

Trichoderma harzianum (Holz and Volkmann, 2002), Rootshield(R) (Marco and 

Osti, 2007) Rifai, 1295-22, (Harman et al., 1996), Trichodex 25 WP 

(Turcanu, 1997) 

Trichoderma virens 31 (Harman et al., 1996) 

Trichosporon pullulans (Holz and Volkmann, 2002) 

Ulocladium atrum, low disease pressure (Metz et al., 2002) (Roudet and Dubos, 

2001) (Schoene et al., 1999) (Holz and Volkmann, 2002) (Lennartz et al., 

1998) (Schoene and Köhl, 1999), isolate 385 (Schoene et al., 2000) 

Ulocladium oudemansii + 5-chlorosalicylic acid in combination (Reglinski et al., 

2005) 


Trichoderma harzianum partial effect (Monchiero et al., 2005) 

Ulocladium oudemansii partial effect (Monchiero et al., 2005) 

Ulocladium atrum, high disease pressure (Metz et al., 2002) (Roudet and Dubos, 

2001) 

Croplife (citrus and coconut extract) + Plantfood (foliar fertilizer), moderate to 

good control (Schilder et al., 2002) 

B 

Milsana (giant knotweed [Fallopia sp.] extract), moderate control (Schilder et al., 

2002) 

O Chitosan (Amborabe et al., 2004) 


Bacteria 

Bacillus sp., (Paul et al., 1998) (Krol, 1998) (Trotel-Aziz et al., 2003), isolate UYBC38 (Rabosto et al., 2006) 

Cupriavidus campinensis (Schoonbeek et al., 2007) 

Pseudomonas sp. (Trotel-Aziz et al., 2003), strain PsJN (Barka et al., 2002) 

Pseudomonas fluorescens (Krol, 1998) 

Pantoea (Trotel-Aziz et al., 2003) 


Alternaria spp., (Walter et al., 2006) 

Aureobasidium pullulans, L47 postharvest (Lima et al., 1997), LS-30 postharvest (Castoria et al., 2001) 

Candida oleophila (Lima et al., 1997), postharvest (El-Neshawy and El-Morsy, 2003) 

Coniothyrium (Sesan et al., 2002) 

Debaryomyces hansenii (Santos et al., 2004) 

Epicoccum spp (Sesan et al., 2002) (Walter et al., 2006) (Fowler et al., 1999) 

Gliocladium, (Sesan et al., 2002) 

Hanseniaspora uvarum (isolate UYNS13) (Rabosto et al., 2006) 

Kloeckera spp. (Cirvilleri et al., 1999) 

Metschnikowia fructicola, postharvest (Karabulut et al., 2003), postharvest (Kurtzman and Droby, 2001) 

Muscodor albus, postharvest (Gabler et al., 2006) 

Pichia anomala (strain FY-102) (Masih et al., 2000) (Santos et al., 2004) 

Pichia membranaefaciens (Masih and Paul, 2002) (Masih et al., 2001) (Santos and Marquina, 2004) (Santos et al., 

2004) 

Scytalidium, (Fowler et al., 1999) 

Trichoderma spp. (Walter et al., 2006) (Fowler et al., 1999) 

Trichoderma harzianum CECT 2413 – mutant (Rey et al., 2001), Rifai postharvest (Batta, 2007) 

Trichoderma viride, (Sesan et al., 2002) 

Trichothecium, (Sesan et al., 2002) 

Tricothecium roseum (Fowler et al., 1999) 

Ulodadium spp (Walter et al., 2006) (Fowler et al., 1999) 

Ulocladium atrum isolate 385 (Schoene et al., 2000) 

Verticillium, (Sesan et al., 2002) 

Oomycetes 

Pythium paroecandrum (Abdelghani et al., 2004) 

Pythium periplocum (Paul, 1999b) 

volatile substances produced by grape cv. Isabella (Vitis labrusca) (postharvest) (Kulakiotu et al., 2004) (Kulakiotu 

and Sfakiotakis, 2003) 

74

Appendix 1 

Strawberry (target pathogen = B. cinerea) 


M 

Bacteria 

Paenibacillus polymyxa 18191 (Helbig, 2001b) 

Pseudomonas fluorescens (Abada et al., 2002) 


Aureobasidium pullulans (Stromeng et al., 2006) 

Candida fructus, (El-Neshawy and Shetaia, 2003) 

C. glabrata, (El-Neshawy and Shetaia, 2003) 

C. oleophila (El-Neshawy and Shetaia, 2003) 

Cryptococcus albidus (Helbig, 2002) 

Epicoccum nigrum, (Stromeng et al., 2006) 

Metschnikowia fructicola (=FG) (Karabulut et al., 2004) 

Pichia guilermondii + Bacillus mycoides mixture (Guetsky et al., 2001) 

(Guetsky et al., 2002) 

Rhodotorula glutinis (Helbig, 2001a) 

Trichoderma harzianum (Abada et al., 2002) (Antoniacci et al., 2000) 

(Maccagnani et al., 1999), 1295-22 (Kovach et al., 2000), (atroviride) P1 

(Hjeljord et al., 2001), T39 (Shafir et al., 2006), Trichodex (Freeman et al., 

2001) (Freeman et al., 2002) (Freeman et al., 2004) 

Trichoderma products (BINAB) (Ricard and Jorgensen, 2000) 

Ulocladium atrum (Boff, 2001) (Boff et al., 2002a) (Boff et al., 2002b) (Köhl et 

al., 2001) (Köhl et al., 2004) (Köhl and Fokkema, 1998) 


Bacillus subtilis (Gengotti et al., 2002) 

Gliocladium roseum (Chaves and Wang, 2004) 

Gliocladium catenulatum, (Prokkola et al., 2003), but low disease incidence 

(Prokkola and Kivijarvi, 2007) 

Trichoderma sp (Stensvand, 1997), (Stensvand, 1998) (Hjeljord et al., 2000) 

(Prokkola et al., 2003), but low disease incidence (Prokkola and Kivijarvi, 

2007) 

Trichoderma harzianum (atroviride) (Hjeljord, 2002) (Hjeljord et al., 2001), 

(Gengotti et al., 2002), Trichodex 40 WP (Meszka and Bielenin, 2004) 


Bacteria 

Bacillus sp. (isolate 17141) (Helbig et al., 1998) 

Bacillus pumilus (Essghaier et al., 2007), NCIMB 13374 (Swadling and Jeffries, 1998) 

Bacillus subtilis, (Essghaier et al., 2007) (Sardi et al., 2008) (Helbig and Bochow, 2001) (Marquenie et al., 1999) 

(Zhao et al., 2007) (Abada et al., 2002) (Gengotti et al., 2000) 

Bacillus marismortui, (Essghaier et al., 2007) 

Bacillus licheniformis, (Essghaier et al., 2007) 

Bacillus thuringiensis (Bacikol) (Kandybin, 2003) 

Virgibacillus marismortui, (Essghaier et al., 2007) 

Enterobacteriaceae (10B1, 5B4) (Guinebretiere et al., 2000) 

Halomonas sp. (Essghaier et al., 2007) 

Pantoea agglomerans strain EPS125, postharvest (Bonaterra et al., 2004) 

Pseudomonas fluorescens (Abada et al., 2002), NCIMB 13373 (Swadling and Jeffries, 1998) 

Pseudomonas cepacia (Marquenie et al., 1999) 

Pseudomonas chlororaphis isolate I-112 (Gulati et al., 1999) 

Pseudomonas syringae but phytotox (Pellegrini et al., 2007) 


Aureo basidium pullulans (Adikaram et al., 2002) 

Candida reukaufii, (Guinebretiere et al., 2000) 

Candida pulcherrima, (Guinebretiere et al., 2000) 

Clonostachys rosea (Cota et al., 2008), IK726 (Mamarabadi et al., 2008) 

Cryptococcus albidus (Helbig, 2002) 

Cryptococcus laurentii (Zheng et al., 2003) 

Gliocladium virens (Tehrani and Alizadeh, 2000) 

Metschnikowia fructicola (Shemer(R) postharvest (Ferrari et al., 2007) 

Pichia guilermondii + Bacillus mycoides mixture (Guetsky et al., 2002b) (Guetsky et al., 2001b) (Guetsky et al., 

2001a) (Guetsky et al., 2002a) 

Rhodotorula glutinis, postharvest (Zhang et al., 2007a), (Helbig, 2001a) 

Trichoderma sp (Santorum et al., 2002) 

Trichoderma harzianum (Abada et al., 2002) (Tehrani and Alizadeh, 2000) (Sanz et al., 2002), T39 (Bilu et al., 

2004) (Levy et al., 2004a) (Levy et al., 2006) (Levy et al., 2004b), atroviride P1 (Hjeljord, Stensvand et al. 

2001) 

Trichoderma asperellum (Sanz et al., 2005) (Sanz et al., 2002) 

Trichoderma longibrachiatum (Sanz et al., 2002) 

Trichoderma atroviride (Sanz et al., 2002) 

Trichoderma koningii, (Tehrani and Alizadeh, 2000) 

Trichoderma viride (Tehrani and Alizadeh, 2000) 

Ulocladium atrum (Boff, 2001) (Berto et al., 2001) (Boff et al., 2001) 

Verticillium lecanii (Koike et al., 2004) 


Pichia guilermondii (Wszelaki and Mitcham, 2003) 

75


B 

O 

Messenger (harpin), (Meszka and Bielenin, 2004) 


Biosept 33 SL (grapefruit extract) (Meszka and Bielenin, 2004) 

seaweed, garlic, and compost extracts (Prokkola et al., 2003), but low disease 

incidence (Prokkola and Kivijarvi, 2007) 

sodium bicarbonate (Funaro, 1997) 


Biochicol 020 PC (chitosan) (Meszka and Bielenin, 2004) 

silicon (Prokkola et al., 2003), but low disease incidence (Prokkola and Kivijarvi, 

2007) 

Natural volatile compounds : benzaldehyde, methyl benzoate, methyl salicylate, 2-nonanone, 2-hexenal 

diethyl acetal, hexanol, and E-2-hexen-1-ol (Archbold et al., 1997) 

Field vegetables (lettuce, onion, cabbage, melon) (target pathogen = B. cinerea) 


M 

B 

O 

Microsphaeropsis ochracea / onion (Carisse et al., 2006) 

Ulocladium atrum 385, onion (Köhl and Fokkema, 1998) (Köhl et al., 1999) 


Bacteria 

Bacillus subtilis / lettuce (Fiddaman et al., 2000), L-form / Chinese cabbage (Walker et al., 2002), / melon (Wang 

et al., 2008c) 

Brevibacillus brevis / lettuce (McHugh and Seddon, 2001) 

Bacillus amyloliquefaciens/ melon (Wang et al., 2008c) 

Pseudomonas spp. (LC8, PF13, PF14, PF15), /lettuce (Card et al., 2002) 

Pseudomonas syringae pv. phaseolicola / Chinese cabbage (Daulagala and Allan, 2003) 

Fungus + yeast: 

Clonostachys rosea / onion (Nielsen et al., 2000) (Yohalem et al., 2004) 

Coniothyrium minitans / lettuce (Fiume and Fiume, 2005) 

Epicoccum sp. (E21) /lettuce (Card et al., 2002) 

Gliocladium virens [Trichoderma virens], / lettuce (Lolas et al., 2005) 

Penicillium griseofulvum, / onion (Tylkowska and Szopinska, 1998) 

Penicillium sp. 90/22, / onion (Tylkowska and Szopinska, 1998) 

Pichia onychis /onion postharvest (German Garcia et al., 2001) (Cotes, 2001) 

Ulocladium sp. (U13), /lettuce (Card et al., 2002) 

Ulocladium atrum / onion (Köhl et al., 2003), 385 and 302 / onion (Nielsen et al., 2000) (Yohalem et al., 2004) 

Trichoderma harzianum, / onion (Tylkowska and Szopinska, 1998), T39 / lettuce (Meyer et al., 1998) (Lolas et al., 

2005), 'Supresivit' / cress (Borregaard, 2000) 

Trichoderma koningii / onion (Tylkowska and Szopinska, 1998) 

T. viride / onion (Tylkowska and Szopinska, 1998) 


Trichoderma-Promot / onion (El-Neshawy et al., 1999) 

76

Appendix 1 

Fruits - postharvest (apple, pears, peach, sweet cherry, kiwi) (target pathogen = B. cinerea) 



Bacteria 

Bacillus licheniformis (EN74-1) (Jamalizadeh et al., 2008) 

Bacillus subtilis (Ongena et al., 2005) , GA1 (Toure et al., 2004), Rizo-N (El-Sheikh Aly et al., 2000) 

Bacillus amyloliquefaciens 2TOE, /pears (Mari et al., 1996) 

Bacillus pumilus 3PPE, /pears (Mari et al., 1996) 

Erwinia sp (Floros et al., 1998) 

Pantoea agglomerans (Sobiczewski and Bryk, 1999) (Nunes et al., 2001a) 

Pseudomonas sp (Sobiczewski and Bryk, 1999) 

Pseudomonas syringae Strain ESC-11 BioSave (Janisiewicz and Jeffers, 1997), / pear (Sugar and Benbow, 2002) 

(Benhow and Sugar, 1997), MA-4 (Zhou et al., 2002), CPA5 (Nunes et al., 2007) 

Pseudomonas fluorescens (Mikani et al., 2007) (Mikani et al., 2008) 

Pseudomonas viridiflava (Bryk et al., 1999) 

Rahnella aquatilis (Calvo et al., 2007) 

M 

Bacteria 

Pantoea agglomerans (CPA-2) (Nunes et al., 2002b) (Nunes et al., 2001b) 

Pseudomonas syringae, MA-4, MB-4, MD-3b and NSA-6 (=FG) (Zhou et al., 2001) 


Aureobasidium pullulans, Rhodotorula glutinis and Bacillus subtilis in combination 

(=FG) (Leibinger et al., 1997) 

Candida saitoana (El-Ghaouth et al., 2001a) , with chitosan (Bio-Coat) or lyric enzyme 

(Biocure) (El-Ghaouth et al., 2001b) 

Candida sake strain CPA-1 combined with diphenylamine (Zanella et al., 2003), CPA- 

1 + ammonium molybdate /pear (Nunes et al., 2002a) 

Metschnikowia pulcherrima (Migheli et al., 1997) 

Pichia anomala strain K beta -1,3-glucans and calcium chloride (Jijakli et al., 2002) 


Aureobasidium pullulans (Achbani et al., 2005) (Lima et al., 2005) (Schena et al., 1999), LS-30 (Lima et al., 1999) 

(Lima et al., 2003), + calcium chloride or sodium bicarbonate (Ippolito et al., 2005b) (Ippolito et al., 2005a) 

Candida butyri JCM 1501, (Wagner et al., 2006) 

Candida melibiosica 2515 (Wagner et al., 2006) 

Candida parapsilosis DSM 70125 (Wagner et al., 2006) 

Candida oleophila Aspire (Droby et al., 2003), Aspire/pear (Sugar and Benbow, 2002) (Benhow and Sugar, 1997), 

Aspire + 2% sodium bicarbonate (Wisniewski et al., 2001), strain O (Jijakli, 2000) (Bajji and Jijakli, 2007) 

(Jijakli et al., 2004) (Lahlali et al., 2007), /peach (Karabulut and Baykal, 2004), 

Candida saitoana (El-Ghaouth et al., 2001c) (El-Ghaouth et al., 2000a) (El-Ghaouth et al., 2000b) (El-Ghaouth et 

al., 2001b) 

Candida sake (Vinas et al., 1998) (Nunes et al., 2002d) (Giraud and Crouzet, 2004) (Cook, 2002b), CPA-1 + 

Pantoea agglomerans (Nunes et al., 2002c) 

Candida famata (21-D), (Lima et al., 1999) 

Candida tenuis, (Faten, 2005) 

Candida pulcherrima (Cook, 2002b) 

Cryptococcus laurentii (Benhow and Sugar, 1997) (Zhang et al., 2005) (Zhang et al., 2007b) (Sugar and Benbow, 

2002) (Tian et al., 2004a) (Jing et al., 2008) (Colgan, 1997) (Lima et al., 2005) (Filonow, 1998) + Gibberellic 

acid (Yu and Zheng, 2007), +IAA (Yu et al., 2008), + salicilic acid (Yu et al., 2007), LS28 (Lima et al., 

2006) (Lima et al., 1998) (Lima et al., 1999) (Lima et al., 2003) 

Cryptococcus albidus, (Fan et al., 2001a) (Fan and Tian, 2001) (Tian et al., 2002) 

Cryptococcus humicola (Anderson et al., 1997) (Filonow et al., 1996) 

Cryptococcus infirmo-miniatus (Benhow and Sugar, 1997) (Sugar and Benbow, 2002) 

Debaryomyces hansenii (strain 43E) / citrus (Arras and Arru, 1999) 

Filobasidium floriforme NRRLY7454, (Filonow et al., 1996) 

Galactomyces geotrichum (Cook, 2002b) 

77


B 

O 

Kloeckera apiculata / peach (Karabulut and Baykal, 2003) (Karabulut et al., 2005) 

Metschnikowia pulcherrima (Spadaro et al., 2002) (Piano et al., 1998) (Spadaro et al., 2004), MACH1 (Duraisamy 

et al., 2008) 

Metschnikowia fructicola (Karabulut et al., 2005) 

Muscodor albus (Mercier and Jimenez, 2004) (Ramin et al., 2008) (Schotsmans et al., 2008) 

Penicillium spp. (El-Sheikh Aly et al., 2000) 

Pichia stipitis CBS 5773 (Wagner et al., 2006) 

Pichia anomala strain K (Grevesse et al., 2003) (Jijakli, 2000) (Friel and Jijakli, 2007) (Friel et al., 2007) (Jijakli 

and Lepoivre, 1998) (Lahlali et al., 2007) 

Pichia guilliermondii (29-A), (Lima et al., 1999) 

Rhodotorula glutinis (Sugar and Benbow, 2002) (Benhow and Sugar, 1997) (Lima et al., 2005) (Lima et al., 1998) 

(Sansone et al., 2005), LS-11 (Lima et al., 1999) (Lima et al., 2003), 

Rhodosporidium toruloides NRRL Y1091, (Filonow et al., 1996) 

Sporobolomyces roseus FS-43-238 (Filonow et al., 1996) (Filonow, 1998) 

Saccharomyces cerevisiae, (Faten, 2005) 

Trichoderma harzianum Plant-guard (El-Sheikh Aly et al., 2000), Rifai (Batta, 2004) 

Trichoderma Viride (El-Sheikh Aly et al., 2000), 

Trichosporon sp., (Fan et al., 2001b) (Tian et al., 2002) 

Trichosporon pullulans (Cook, 2002b) 

R. glutinis SL 1 + C. laurentii SL 62 mixture (Calvo et al., 2003) 


Candida oleophila (Aspire), (Colgan, 1997) 

volatile substances produced by grape cv. Isabella (Vitis labrusca) (Kulakiotu and Sfakiotakis, 2003b) (Kulakiotu 

et al., 2004a) 

Chitosan, (Faten, 2005) 

Calcium (Chardonnet et al., 2000) (Holmes et al., 1998) 

Phosphonate (Holmes et al., 1998) 

sodium bicarbonate (Karabulut et al., 2005) 

78

Appendix 1 

Legumes (Fabaceae) (target pathogen = B. cinerea) 


M 

Bacteria 

Bacillus subtilis K-3 / lupin (Kuptsov et al., 2004) 

Pantoea agglomerans / lentil (Huang and Erickson, 2002), LRC 954, / lentil (Huang 

and Erickson, 2005) 

Pseudomonas fluorescens, / lentil (Huang and Erickson, 2002) LRC 1788 / lentil 

(Huang and Erickson, 2005) 


Clonostachys rosea / alfalfa (Li et al., 2004a) 

Gliocladium catenulatum, / alfalfa (Li et al., 2004a) 

Penicillium aurantiogriseum LRC 2450 / lentil (Huang and Erickson, 2005) 

Penicillium griseofulvum / lentil (Huang and Erickson, 2002) 

Trichoderma hamatum / lentil (Huang and Erickson, 2002) 

Trichoderma harzianum LRC 2428 / lentil (Huang and Erickson, 2005) 

Trichoderma viride / chickpea (Abha et al., 1999) 

Trichoderma atroviride, / alfalfa (Li et al., 2004a) 

Trichothecium roseum / alfalfa (Li et al., 2004a) 

Mixture: Streptomyces exfoliatus + Trichoderma harzianum / faba bean (Mahmoud et 

al., 2004) 

B Eucalyptus citriodora + Ipomoea carnea extracts / faba bean (Mahmoud et al., 2004) 

O 


Bacteria 

Bacillus subtilis (Saad et al., 2005) 

Bacillus megaterium (Saad et al., 2005) 

Bacillus cereus (Kishore and Pande, 2007) 

Bacillus macerans BS 153 (Sharga, 1997) 

Pantoea agglomerans (Huang and Erickson, 2002), LRC 954, (Huang and Erickson, 2005) 

Pseudomonas fluorescens, (Huang and Erickson, 2002) LRC 1788 (Huang and Erickson, 2005) 

Pseudomonas putida BTP1 (Ongena et al., 2002) 

Streptomyces albaduncus (Razak et al., 2000) 

Streptomyces griseoplanus (Razak et al., 2000) 

Streptomyces violaceus T118 (Ahmad et al., 2002) 


Botrytis cinerea non-aggressive strains /bean leaves (Weeds et al., 2000) 

Chaetomium globosum (Pradeep et al., 2000) 

Cladosporium cladosporioides (Jackson et al., 1997) 

Epicoccum nigrum, (Szandala and Backhouse, 2001) 

Gliocladium roseum (Li et al., 2002) (Szandala and Backhouse, 2001) (Burgess and Keane, 1997) 

Penicillium brevicompactum (Jackson et al., 1997) 

Penicillium aurantiogriseum LRC 2450 (Huang and Erickson, 2005) 

Penicillium griseofulvum (Huang and Erickson, 2002) 

Trichoderma (Burgess and Keane, 1997) 

Trichoderma harzianum (Szandala and Backhouse, 2001), T39 (Bigirimana et al., 1997) (Kapat et al., 1998) (Elad 

et al., 2004), LRC 2428 (Huang and Erickson, 2005) 

Trichoderma viride /pigeon pea (Pradeep et al., 2000), / chickpea (Abha and Tripathi, 1999) (Mukherjee et al., 

1997) 

Trichoderma hamatum (Huang and Erickson, 2002) 

extracts from green parts of tomato, potato, rape (Smolinska and Kowalska, 2006) 

pterocarpan phytoalexin maackiain from chickpea (Stevenson and Haware, 1999) 

79


Flowers (target pathogen = B. cinerea) 



Bacteria 

Bacillus amyloliquefaciens / lily (Chiou and Wu, 2001) 

Bacillus subtilis / rose buds (Tatagiba et al., 1998) 

Burkholderia gladioli, / lily (Chiou and Wu, 2001) 

Pseudomonas sp. 677 /geraldton waxflower (Beasley et al., 2001) 

Serratia marcescens strain B2 / cyclamen (Someya et al., 2001) 

M 

B 

O 

Bacteria 

Bacillus amyloliquefaciens B190 / lily (Chiou and Wu, 2003) 

Bacillus cereus / lily (Liu et al., 2008) 

Bacillus amyloliquefaciens / lily (Chiou and Wu, 2001) 

Burkholderia gladioli, / lily (Chiou and Wu, 2001) 

Pseudomonas putida / lily (Liu et al., 2008) 


Clonostachys rosea /rose (Morandi et al., 2003) 

Ulocladium atrum / cyclamen (Köhl et al., 2000) (Köhl et al., 1998) 


Trichoderma harzianum / cyclamen (Minuto et al., 2002) (Minuto et al., 2004) 

Fungi + yeasts 

Cladosporium spp. / rose (Morandi et al., 1999) 

Cladosporium oxysporum, / rose debris + buds (Tatagiba et al., 1998) 

Cladosporium cladosporioides / rose buds (Tatagiba et al., 1998) 

Clonostachys rosea /rose (Morandi et al., 1999) (Morandi et al., 2006) (Morandi et al., 2001) (Morandi et al., 

2007) (Morandi et al., 2008) (Morandi et al., 2000b) (Morandi et al., 2000a) (Yohalem, 2004) (Yohalem, 

2000) 

Epicoccum sp. / Geraldton waxflower (Beasley et al., 2001) 

Fusarium sp., / Geraldton waxflower (Beasley et al., 2001) 

Gliocladium roseum FR136 / rose debris (Tatagiba et al., 1998) 

Rhizoctonia (BNR), / geranium (Olson and Benson, 2007) 

Rhodotorula glutinis PM4 / geranium (Buck and Jeffers, 2004) (Buck, 2004) 

Rhodotorula graminis, / geranium (Buck, 2004) 

Rhodotorula Mucilaginosa / geranium (Buck, 2004) 

Trichoderma spp / Geraldton waxflower (Beasley et al., 2001) 

Trichoderma harzianum (Trichodex) / Geraldton waxflower (Beasley et al., 2005) 

Trichoderma hamatum / statice (Diaz et al., 1999), 382 / geranium (Olson and Benson, 2007) 

Trichoderma inhamatum, / rose debris (Tatagiba et al., 1998) 

Ulocladium atrum / cyclamen (Kessel, 1999) (Kessel et al., 2001) (Kessel et al., 2005) (Köhl and Molhoek, 2001) 

(Kessel et al., 2002) (Kessel et al., 1999), /lily (Kessel et al., 1999) (Elmer and Köhl, 1998) (Kessel et al., 

2001), / geranium (Gerlagh et al., 2001), / rose (Yohalem and Kristensen, 2004) (Yohalem, 2004) (Köhl and 

Gerlagh, 1999) (Yohalem et al., 2007) (Yohalem, 2000), / pelargonium (Yohalem et al., 2007) 


Trichoderma hamatum 382 in compost / begonia (Horst et al., 2005) 

Trichoderma harzianum preparations (Yohalem, 2000) (Trichodex and Supresivit) (Yohalem, 2004) 

grapefruit [Citrus paradisi] extract / lily, peony and tulip (Orlikowski et al., 2002), / tulips, Gerbera jamesonii and 

carnations (Orlikowski and Skrzyoczak, 2003), Biosept 33 SL / tulip (Orlikowski and Skrzypczak, 2001) 

chitosan / tulips, Gerbera jamesonii and carnations (Orlikowski and Skrzyoczak, 2003) 

80

Appendix 1 

Miscellaneous crops (target pathogen = B. cinerea) 


M 

Bacteria 

Streptomyces griseoviridis (Mycostop) / Pinus sylvestris (Capieau et al., 2001) 

(Capieau et al., 2004) 


Gliocladium sp (GlioMix) / Pinus sylvestris (Capieau et al., 2001) (Capieau et al., 

2004) 

Gliocladium roseum / Eucalyptus nurseries (Stowasser and Ferreira, 1997) 

Trichoderma harzianum and T. polysporum (Binab TF.WP), / Pinus sylvestris (Capieau 

et al., 2001) (Capieau et al., 2004) 

Trichoderma viride (Trichosemin 25 PTS (25% Tv), / sunflower (Eva, 2003) 


Penicillium sp. / Eucalyptus nurseries (Stowasser and Ferreira, 1997) 

Trichoderma harzianum , Trichoderma viride / Eucalyptus nurseries (Stowasser and 

Ferreira, 1997) 


Bacteria 

Bacillus spp./ Ginseng (Kim et al., 1997) (Chung et al., 1998) 

Bacillus subtilis Cot1 and CL27 / Astilbe hybrida, Aster hybrida, Daphne blayana, Photinia fraseri (Li et al., 1998) 

Bacillus amyloliquefaciens / oilseed rape (Danielsson et al., 2007) 

Bacillus licheniformis / Perilla (Son et al., 2002) 

B. megaterium / Perilla (Son et al., 2002) 

Cupriavidus campinensis / Arabidopsis thaliana (Schoonbeek et al., 2007) 

Erwinia / Ginseng (Kim et al., 1997) 

Pseudomonas fluorescens / castor crop (Raoof et al., 2003), WCS374r / Eucalyptus (Ran et al., 2005) 

Pseudomonas putida WCS358r / Eucalyptus (Ran et al., 2005) 

Streptomyces griseoviridis (Mycostop) / Pinus sylvestris (Capieau et al., 2001) (Capieau et al., 2004) 


Clonostachys (A-10) / Pinus radiate, Eucalyptus globulus (Molina Mercader et al., 2006) 

Cylindrocladium spp. / Eucalyptus (Fortes et al., 2007) 

Gliocladium sp (GlioMix) / Pinus sylvestris (Capieau et al., 2001) (Capieau et al., 2004) 

Gliocladium roseum / Picea mariana (Zhang et al., 1996) 

Trichoderma spp. / Eucalyptus (Fortes et al., 2007) 

Trichoderma harzianum / Arabidopsis thaliana (Korolev and Elad, 2004) / castor crop (Tirupathi et al., 2006) 

(Raoof et al., 2003) (Bhattiprolu and Bhattiprolu, 2006), / hazelnut (Machowicz-Stefaniak et al., 2004) 

Trichoderma viride / castor crop (Tirupathi et al., 2006) (Raoof et al., 2003) (Bhattiprolu and Bhattiprolu, 2006), T 

13-82 (Trichodermin-BL) / flax (Pristchepa et al., 2006), / hazelnut (Machowicz-Stefaniak et al., 2004) 

Trichoderma harzianum and T. polysporum (Binab TF.WP), / Pinus sylvestris (Capieau et al., 2001) (Capieau et 

al., 2004) 

B Mature leaf extract of Lantana camera / castor crop (Bhattiprolu and Bhattiprolu, 2006) 

O Cryptogein, elicitor secreted by Phytophthora cryptogea / tobacco (Blancard et al., 1998) 

81


Successful inhibition in vitro (target pathogen = B. cinerea) 

Bacteria 

Alcaligenes faecalis (Honda et al., 1999) 

Azotobacter (Khan et al., 2006) 

Bacillus sp mutant strain (Bernal et al., 2002) 

Bacillus amyloliquefaciens CCMI 1051 (Caldeira et al., 2007), BL-3 (Lee et al., 2001) 

Bacillus brevis [Brevibacillus brevis](Gu et al., 2001) (Edwards and Seddon, 2001) 

Bacillus cereus (Guven et al., 2008) (Huang and Chen, 2004) 

Bacillus circulans (Paul et al., 1997) 

Bacillus licheniformis W10 (Ji et al., 2007) (Gu et al., 2001) 

Bacillus subtilis (Gu et al., 2001) (Chen et al., 2008) (Chen et al., 2004b) (Zhao et al., 2003) (Chen et al., 2004a) (Zakharchenko et al., 2007) (Gu et al., 2004) (Novikova et al., 2003) (Hsieh et al., 

2003) (Feng et al., 2003) (Liu et al., 2007b) 

Bacillus thuringiensis CMB26 (Kim et al., 2004) 

Paenibacillus polymyxa BL-4 (Lee et al., 2001) 

Photorhabdus luminescens ATCC 29999 (Hsieh et al., 2004) 

Plutella xylostella (Indiragandhi et al., 2008) 

Pseudomonas (Lian et al., 2007) (Cornea et al., 2007) (Kim et al., 2000) (Woo et al., 2002) (Bryk et al., 2004) 

Pseudomonas aeruginosa PUPa3 (Kumar et al., 2005) 

Pseudomonas antimicrobica (Walker et al., 2001) 

Pseudomonas corrugata strain P94 (Guo et al., 2007) 

Pseudomonas fluorescens (Nian et al., 2007) (Khan and Almas, 2002) 

Pseudomonas putida (Cornea et al., 2007), Cha 94 (Lee et al., 2001) 

M 

Pseudomonas syringae pv. syringae strain B359 (Fogliano et al., 2002) 

Lysobacter capsici sp. Nov (Park et al., 2008) 

Serratia plymuthica C48 (Frankowski et al., 2001a) (Frankowski et al., 2001b) 

Streptomyces + actinomycetes (Tian et al., 2004b) (Nadkarni et al., 1998) (Liang et al., 2007, Yan et al., 2004) (Han et al., 2004) (Liang et al., 2007) (Long et al., 2005) (Stoppacher et al., 2007) (Kim 

et al., 2007b) 

Streptomyces ahygroscopicus (Sun et al., 2003) (Yang et al., 2007) (Zhao et al., 1998) 

Streptomyces luteogriseus ECO 00001 (Li et al., 2008) 

Streptomyces rimosus subsp. daheishanensis strain MY02 (Liu et al., 2004) 

Streptomyces roseoflavus strain LS-A24 (Park et al., 2006) 

Tripterygiun wilfordii (Shentu et al., 2006) 

Xenorhabdus sp. strain CB43 (Xiao et al., 2005) 

Xenorhabdus nematophilus YL001 (Liu et al., 2006) 

marine bacteria (Nie et al., 2007) 


Acremonium strictum (Kim et al., 2002) 

Aspergillus fumigatus and A. terreus (El-Zayat, 2008) 

Aspergillus clavatonanicus (Zhang et al., 2008) 

Cryptococcus laurentii (isolate LS-28) (Castoria et al., 1997) 

Fusarium lateritium extracts (Anitha, 2006) 

Fusarium semitectum (Altomare et al., 2000) 

82

Appendix 1 

Lecanicillium muscarium (Fenice and Gooday, 2006) 

Muscodor albus (Mercier and Jimenez, 2007) 

Rhodotorula (Calvente et al., 2001) 

Rhodotorula glutinis (Castoria et al., 1997) 

Trichoderma (Pezet et al., 1999) (Chen et al., 2005) (Liu et al., 2007a) 

Trichoderma viride (Machowicz-Stefaniak, 1998) T15 and T17 (Silva-Ribeiro et al., 2001) 

Trichoderma atroviride (Navazio et al., 2007) (Klemsdal et al., 2006) GMO (Brunner et al., 2005) 

Trichoderma harzianum (Dana et al., 2001) (Ding et al., 2002) (Limon et al., 2004) (Mach et al., 1999) T5A, T1 and T1A (Silva-Ribeiro et al., 2001) (Lee et al., 2001), T-33 (Witkowska and Maj, 

2002) 

Trichoderma hamatum C-1 (Witkowska and Maj, 2002) 

Trichoderma reesei [T. longibractiatum] M7-1 (Witkowska and Maj, 2002) 

Oomycetes 

Pythium bifurcatum (Paul, 2003) 

Pythium citrinum (Paul, 2004) 

Pythium contiguanum (Paul, 2000) 

Pythium radiosum (Paul, 1999a) 

B 

O 

Antifungal metabolites of endophytic fungus, A10 (Qian et al., 2006) 

antimicrobial peptide Ar-AMP from Amaranthus retroflexus L. (Lipkin, Anisimova et al. 2005) 

basic haem-peroxidase (WP1) from wheat (Triticum aestivum) kernels (Caruso, Chilosi et al. 2001) 

Extracts from Bazzania trilobata, Diplophyllum albicans, Sphagnum quinquefarium, Dicranodontium denudatum and Hylocomium splendens (Tadesse, Steiner et al. 2003) 

Extracts of Sophora flavescens (Zheng et al., 2000) (Zheng et al., 1999) 

Irpex lacteus (Fr.) Fr., Trametes versicolor (L.:Fr.) Pilat, and Chondrostereum purpureum (Pers.:Fr.) Pouzar (White and Traquair, 2006) 

Pyrrolnitrin, produced by several bacteria (Okada et al., 2005) 

Ten sesquiterpenes and six diterpenes from Pilgerodendron uviferum wood and bark (Solis et al., 2004) 

chlorine dioxide (Zoffoli et al., 2005) 

earthworm (Eisenia fetida) polysaccharides (Wang et al., 2007b) 

chitosan derivatives (Rabea et al., 2003) 

83


References on biocontrol against Botrytis 

Abada, K. A., Wahdan, H. M., and Abdel-Aziz, M. A. (2002). Fungi associated with fruit-rots of fresh strawberry plantations and some trials of their control. Bulletin of Faculty of Agriculture, Cairo 

University 53, 309-326. 

Abdelghani, E. Y., Bala, K., and Paul, B. (2004). Characterisation of Pythium paroecandrum and its antagonism towards Botrytis cinerea, the causative agent of grey mould disease of grape. FEMS 

Microbiology Letters 230, 177-183. 

Abha, A., and Tripathi, H. S. (1999). Biological and chemical control of Botrytis gray mould of chickpea. Journal of Mycology and Plant Pathology 29, 52-56. 

Abha, A., Tripathi, H. S., and Rathi, Y. P. S. (1999). Integrated management of grey mould of chickpea. Journal of Mycology and Plant Pathology 29, 116-117. 

Acar, O., Aki, C., and Erdugan, H. (2008). Fungal and bacterial diseases control with ElexaTM plant booster. Fresenius Environmental Bulletin 17, 797-802. 

Achbani, E. H., Mounir, R., Jaafari, S., Douira, A., Benbouazza, and Jijakli, M. H. (2005). Selection of antagonists of postharvest apple parasites: Penicillium expansum and Botrytis cinerea. Communications 

in Agricultural and Applied Biological Sciences 70, 143-149. 

Adikaram, N. K. B., Joyce, D. C., and Terry, L. A. (2002). Biocontrol activity and induced resistance as a possible mode of action for Aureobasidium pullulans against grey mould of strawberry fruit. 

Australasian Plant Pathology 31, 223-229. 

Ahmad, M. S., Abou-Zeid, N. M., Swelim, M. A., Yassin, M. H., and Daboor, S. M. (2002). Characterization of an antibiotic produced by Streptomyces violaceus T118 and its effect in controlling chocolate 

spot disease of Faba bean plant. Egyptian Journal of Microbiology 37, 197-212. 

Allan, E. J., Lazaraki, I., Dertzakis, D., Woodward, S., Seddon, B., and Schmitt, A. (2003). Integrated biological control of powdery mildew and grey mould of cucumber and tomato using Brevibacillus brevis 

combinations. In "The BCPC International Congress: Crop Science and Technology, Volumes 1 and 2. Proceedings of an international congress held at the SECC, Glasgow, Scotland, UK, 10-12 

November 2003", pp. 469-474. 

Altomare, C., Perrone, G., Zonno, M. C., Evidente, A., Pengue, R., Fanti, F., and Polonelli, L. (2000). Biological characterization of fusapyrone and deoxyfusapyrone, two bioactive secondary metabolites of 

Fusarium semitectum. Journal of Natural Products 63, 1131-1135. 

Amborabe, E., Aziz, A., Trotel-Aziz, P., Quantinet, D., Dhuicq, L., and Vernet, G. (2004). Chitosan against Botrytis cinerea on vineyard. Phytoma, 26-29. 

Anderson, J. A., Filonow, A. B., and Vishniac, H. S. (1997). Cryptococcus humicola inhibits development of lesions in 'Golden Delicious' apples. HortScience 32, 1235-1236. 

Anitha, R. (2006). Antifungal activity of Fusarium lateritium extracts. Indian Journal of Microbiology 46, 73-75. 

Antoniacci, L., Cobelli, L., Paoli, E. d., and Gengotti, S. (2000). Open field control trials against strawberry grey mould. Informatore Fitopatologico 50, 45-51. 

Apablaza, H. G., and Jalil R, C. (1998). Trichoderma harzianum and pyrimethanil efficiency to control tomato gray mold (Botrytis cinerea) in greenhouse production. Ciencia e Investigacion Agraria 25, 51- 

58. 

Archbold, D. D., Hamilton-Kemp, T. R., Langlois, B. E., and Barth, M. M. (1997). Natural volatile compounds control Botrytis on strawberry fruit. Acta Horticulturae, 923-930. 

Arras, G., and Arru, S. (1999). Integrated control of postharvest citrus decay and induction of phytoalexins by Debaryomyces hansenii. Advances in Horticultural Science 13, 76-81. 

Audenaert, K., Damme, A. v., Cornelis, P., Cornelis, T., and Hofte, M. (2002). Induced resistance by Pseudomonas aeruginosa 7NSK2: bacterial determinants and reactions in the plant. Bulletin OILB/SROP 

25, 223-226. 

Bajji, M., and Jijakli, M. H. (2007). Wound age effect on the efficacy of Candida oleophila strain O against post-harvest decay of apple fruits. Bulletin OILB/SROP 30, 279-282. 

Barakat, R. M., and Al-Masri, M. I. (2005). Biological control of gray mold disease (Botrytis cinerea) on tomato and bean plants by using local isolates of Trichoderma harzianum. Dirasat. Agricultural 

Sciences 32, 145-156. 

Bardin, M., Fargues, J., Couston, L., Troulet, C., Philippe, G., and Nicot, P. C. (2004a). Combined biological control against 3 bioaggressors of tomato. PHM Revue Horticole, 36-39. 

Bardin, M., Fargues, J., Couston, L., Troulet, C., Philippe, G., and Nicot, P. C. (2004b). Compatibility of intervention to control grey mould, powdery mildew and whitefly on tomato, using three biological 

methods. Bulletin OILB/SROP 27, 5-9. 

Bardin, M., Fargues, J., and Nicot, P. C. (2008). Compatibility between biopesticides used to control grey mould, powdery mildew and whitefly on tomato. Biological Control 46, 476-483. 

Barka, E. A., Gognies, S., Nowak, J., Audran, J. C., and Belarbi, A. (2002). Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biological Control 24, 

135-142. 

Batta, Y. A. (2004). Postharvest biological control of apple gray mold by Trichoderma harzianum Rifai formulated in an invert emulsion. Crop Protection 23, 19-26. 

Batta, Y. A. (2007). Control of postharvest diseases of fruit with an invert emulsion formulation of Trichoderma harzianum Rifai. Postharvest Biology and Technology 43, 143-150. 

Beasley, D. R., Joyce, D. C., Coates, L. M., and Wearing, A. H. (2001). Saprophytic microorganisms with potential for biological control of Botrytis cinerea on Geraldton waxflower flowers. Australian 

Journal of Experimental Agriculture 41, 697-703. 

Beasley, D. R., Joyce, D. C., Wearing, A. H., and Coates, L. M. (2005). Bees as biocontrol agent delivery vectors: a preliminary study for Geraldton waxflower flowers. Acta Horticulturae, 421-424. 

84

Appendix 1 

Bedini, S., Bagnoli, G., Sbrana, C., Leporini, C., Tola, E., Dunne, C., Filippi, C., D'Andrea, F., O'Gara, F., and Nuti, M. P. (1999). Pseudomonads isolated from within fruit bodies of Tuber borchii are capable 

of producing biological control or phytostimulatory compounds in pure culture. Symbiosis (Rehovot) 26, 223-236. 

Bello, G. d., Monaco, C., Rollan, M. C., Lampugnani, G., Arteta, N., Abramoff, C., Ronco, L., and Stocco, M. (2008). Biocontrol of postharvest grey mould on tomato by yeasts. Journal of Phytopathology 

156, 257-263. 

Benhow, J. M., and Sugar, D. (1997). High CO2 CA storage combined with biocontrol agents to reduce postharvest decay of pear. Postharvest Horticulture Series - Department of Pomology, University of 

California, 270-276. 

Benuzzi, M., Ladurner, E., and Fiorentini, F. (2006). Efficacy of Serenade, new Bacillus subtilis-based biofungicide, in controlling the pathogenic microorganisms of crops. In "Giornate Fitopatologiche 2006, 

Riccione", pp. 429-436. 

Bernal, G., Illanes, A., and Ciampi, L. (2002). Isolation and partial purification of a metabolite from a mutant strain of Bacillus sp. with antibiotic activity against plant pathogenic agents. EJB, Electronic 

Journal of Biotechnology 5, 1-7. 

Berto, P., Jijakli, M. H., and Lepoivre, P. (2001). Possible role of colonization and cell wall-degrading enzymes in the differential ability of three Ulocladium atrum strains to control Botrytis cinerea on 

necrotic strawberry leaves. Phytopathology 91, 1030-1036. 

Bhattiprolu, S. L., and Bhattiprolu, G. R. (2006). Management of castor grey rot disease using botanical and biological agents. Indian Journal of Plant Protection 34, 101-104. 

Bigirimana, J., Meyer, G. d., Poppe, J., Elad, Y., and Hofte, M. (1997). Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum. Mededelingen - Faculteit Landbouwkundige 

en Toegepaste Biologische Wetenschappen, Universiteit Gent 62, 1001-1007. 

Bilu, A., David, D. R., Dag, A., Shafir, S., Abu-Toamy, M., and Elad, Y. (2004). Using honeybees to deliver a biocontrol agent for the control of strawberry Botrytis cinerea-fruit rots. Bulletin OILB/SROP 27, 

17-21. 

Blancard, D., Coubard, C., Bonnet, P., Lenoir, M., and Ricci, P. (1998). Induction of an unspecific protection against 5 pathogenic fungi in stem and leaves of tobacco plants elicited by cryptogein. Annales du 

Tabac. Section 2, 11-20. 

Bocchese, C. A. C., Lisboa, B. B., Silveira, J. R. P., Vargas, L. K., Radin, B., and Oliveira, A. M. R. d. (2007). Selection of antagonists for the biological control of Botrytis cinerea in tomato grown under 

protected cultivation. Pesquisa Agropecuaria Gaucha 13, 29-38. 

Boff, P. (2001). Epidemiology and biological control of grey mould in annual strawberry crops. In "Epidemiology and biological control of grey mould in annual strawberry crops", pp. vii + 128 pp. 

Boff, P., Köhl, J., Gerlagh, M., and Kraker, J. d. (2002a). Biocontrol of grey mould by Ulocladium atrum applied at different flower and fruit stages of strawberry. BioControl 47, 193-206. 

Boff, P., Köhl, J., Jansen, M., Horsten, P. J. F. M., Plas, C. L. v. d., and Gerlagh, M. (2002b). Biological control of gray mold with Ulocladium atrum in annual strawberry crops. Plant Disease 86, 220-224. 

Boff, P., Kraker, J. d., Bruggen, A. H. C. v., Gerlagh, M., and Köhl, J. (2001). Conidial persistence and competitive ability of the antagonist Ulocladium atrum on strawberry leaves. Biocontrol Science and 

Technology 11, 623-636. 

Bonaterra, A., Frances, J. M., Moreno, M. C., Badosa, E., and Montesinos, E. (2004). Post-harvest biological control of a wide range of fruit types and pathogens by Pantoea agglomerans EPS125. Bulletin 

OILB/SROP 27, 357-360. 

Borregaard, S. (2000). Supresivit (Trichoderma harzianum): "Evaluation of effect-trials". DJF Rapport, Havebrug, 63-65. 

Brunner, K., Zeilinger, S., Ciliento, R., Woo, S. L., Lorito, M., Kubicek, C. P., and Mach, R. L. (2005). Improvement of the fungal biocontrol agent Trichoderma atroviride to enhance both antagonism and 

induction of plant systemic disease resistance. Applied and Environmental Microbiology 71, 3959-3965. 

Bryk, H., Dyki, B., and Sobiczewski, P. (2004). Inhibitory effect of Pseudomonas spp. on the development of Botrytis cinerea and Penicillium expansum. Plant Protection Science 40, 128-134. 

Bryk, H., Sobiczewski, P., and Berczynski, S. (1999). Evaluation of protective activity of epiphytic bacteria against gray mold (Botrytis cinerea) and blue mold (Penicillium expansum) on apples. 

Phytopathologia Polonica, 69-79. 

Buck, J. W. (2004). Combinations of fungicides with phylloplane yeasts for improved control of Botrytis cinerea on geranium seedlings. Phytopathology 94, 196-202. 

Buck, J. W., and Jeffers, S. N. (2004). Effect of pathogen aggressiveness and vinclozolin on efficacy of Rhodotorula glutinis PM4 against Botrytis cinerea on geranium leaf disks and seedlings. Plant Disease 

88, 1262-1268. 

Burgess, D. R., and Keane, P. J. (1997). Biological control of Botrytis cinerea on chickpea seed with Trichoderma spp. and Gliocladium roseum: indigenous versus non-indigenous isolates. Plant Pathology 

46, 910-918. 

Caldeira, A. T., Feio, S. S., Arteiro, J. M. S., and Roseiro, J. C. (2007). Bacillus amyloliquefaciens CCMI 1051 in vitro activity against wood contaminant fungi. Annals of Microbiology 57, 29-33. 

Calvente, V., Orellano, M. E. d., Sansone, G., Benuzzi, D., and Sanz de Tosetti, M. I. (2001). Effect of nitrogen source and pH on siderophore production by Rhodotorula strains and their application to 

biocontrol of phytopathogenic moulds. Journal of Industrial Microbiology & Biotechnology 26, 226-229. 

Calvo, J., Calvente, V., Orellano, M. E. d., Benuzzi, D., and Sanz de Tosetti, M. I. (2003). Improvement in the biocontrol of postharvest diseases of apples with the use of yeast mixtures. BioControl 48, 579- 

593. 

85


Calvo, J., Calvente, V., Orellano, M. E. d., Benuzzi, D., and Sanz de Tosetti, M. I. (2007). Biological control of postharvest spoilage caused by Penicillium expansum and Botrytis cinerea in apple by using the 

bacterium Rahnella aquatilis. International Journal of Food Microbiology 113, 251-257. 

Capieau, K., Stenlid, J., and Stenstrom, E. (2004). Potential for biological control of Botrytis cinerea in Pinus sylvestris seedlings. Scandinavian Journal of Forest Research 19, 312-319. 

Capieau, K., Stenstrom, E., and Stenlid, J. (2001). Biological control of Botrytis cinerea of pine seedlings in a forest nursery in Sweden. Bulletin OILB/SROP 24, 185. 

Card, S., Jaspers, M. V., Walter, M., and Stewart, A. (2002). Evaluation of micro-organisms for biocontrol of grey mould on lettuce. In "New Zealand Plant Protection Volume 55, 2002. Proceedings of a 

conference, Centra Hotel, Rotorua, New Zealand, 13-15 August 2002", pp. 197-201. 

Carisse, O., Rolland, D., and Tremblay, D. M. (2006). Effect of Microsphaeropsis ochracea on production of sclerotia-borne and airborne conidia of Botrytis squamosa. BioControl 51, 107-126. 

Castoria, R., Curtis, F. d., Lima, G., Caputo, L., Pacifico, S., and Cicco, V. d. (2001). Aureobasidium pullulans (LS-30) an antagonist of postharvest pathogens of fruits: study on its modes of action. 

Postharvest Biology and Technology 22, 7-17. 

Castoria, R., Curtis, F. d., Lima, G., and Cicco, V. d. (1997). beta -1,3-Glucanase activity of two saprophytic yeasts and possible mode of action as biocontrol agents against postharvest diseases. Postharvest 

Biology and Technology 12, 293-300. 

Cayuela, M. L., Millner, P. D., Meyer, S. L. F., and Roig, A. (2008). Potential of olive mill waste and compost as biobased pesticides against weeds, fungi, and nematodes. Science of the Total Environment 

399, 11-18. 

Chardonnet, C. O., Sams, C. E., Trigiano, R. N., and Conway, W. S. (2000). Variability of three isolates of Botrytis cinerea affects the inhibitory effects of calcium on this fungus. Phytopathology 90, 769-774. 

Chaves, N., and Wang, A. (2004). Control of gray mold (Botrytis cinerea) in strawberry with Gliocladium roseum. Agronomia Costarricense 28, 73-85. 

Chen, C., Wang, Y., and Huang, C. (2004a). Enhancement of the antifungal activity of Bacillus subtilis F29-3 by the chitinase encoded by Bacillus circulans chiA gene. Canadian Journal of Microbiology 50, 

451-454. 

Chen, H., Chen, J., Kan, G., and Li, H. (2005). Mutation of Trichoderma in tolerance to pyrimethanil and induction of related protein. Acta Phytophylacica Sinica 32, 77-80. 

Chen, H., Xiao, X., Wang, J., Wu, L., Zheng, Z., and Yu, Z. (2008). Antagonistic effects of volatiles generated by Bacillus subtilis on spore germination and hyphal growth of the plant pathogen, Botrytis 

cinerea. Biotechnology Letters 30, 919-923. 

Chen, L., Tan, G., and Ding, K. (2004b). Inhibiting effect of Bacillus subtilis on four Botrytis cinerea. Journal of Fungal Research 2, 44-47. 

Cherif, M., and Boubaker, A. (1998). Effects of cultural practices, fungicides and biocontrol agents on Botrytis bunch rot of grapes. Bulletin OILB/SROP 21, 41-51. 

Chiou, A. L., and Wu, W. S. (2001). Isolation, identification and evaluation of bacterial antagonists against Botrytis elliptica on lily. Journal of Phytopathology 149, 319-324. 

Chiou, A. L., and Wu, W. S. (2003). Formulation of Bacillus amyloliquefaciens B190 for control of lily grey mould (Botrytis elliptica). Journal of Phytopathology 151, 13-18. 

Chung, H., Chung, E., and Lee, Y. (1998). Biological control of postharvest root rots of ginseng. Korean Journal of Plant Pathology 14, 268-277. 

Cirvilleri, G., Catara, V., Bella, P., and Coco, V. (1999). Evaluation of yeasts for biological control of grey mould on table grape. Phytophaga (Palermo) 9, 89-96. 

Colgan, R. J. (1997). Reducing the reliance on post-harvest fungicides to control storage rots of apples and pears. Bulletin OILB/SROP 20, 69-76. 

Cook, D. W. M. (2002a). Effect of formulated yeast in suppressing the liberation of Botrytis cinerea conidia. Plant Disease 86, 1265-1270. 

Cook, D. W. M. (2002b). A laboratory simulation for vectoring of Trichosporon pullulans by conidia of Botrytis cinerea. Phytopathology 92, 1293-1299. 

Cornea, C. P., Lupescu, I., Voaides, C., Groposila, D., Ciuca, M., Eremia, M., Popa, G., and Ilie, B. (2007). Polyhydroxyalkanoates biosynthesis in new bacterial strains with antimicrobial properties. Bulletin 

of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Animal Science and Biotechnologies 63/64, 540. 

Cota, L. V., Maffia, L. A., and Mizubuti, E. S. G. (2008). Brazilian isolates of Clonostachys rosea: colonization under different temperature and moisture conditions and temporal dynamics on strawberry 

leaves. Letters in Applied Microbiology 46, 312-317. 

Cotes, A. M. (2001). Biocontrol of fungal plant pathogens - from the discovery of potential biocontrol agents to the implementation of formulated products. Bulletin OILB/SROP 24, 43-47. 

Dana, M., Benitez, T., Kubicek, C. P., and Pintor-Toro, J. A. (2001). Chitinase 33 gene expression in Trichoderma harzianum during mycoparasitism. Bulletin OILB/SROP 24, 363. 

Danielsson, J., Reva, O., and Meijer, J. (2007). Protection of oilseed rape (Brassica napus) toward fungal pathogens by strains of plant-associated Bacillus amyloliquefaciens. Microbial Ecology 54, 134-140. 

Daulagala, P. W. H. K. P., and Allan, E. J. (2003). L-form bacteria of Pseudomonas syringae pv. phaseolicola induce chitinases and enhance resistance to Botrytis cinerea infection in Chinese cabbage. 

Physiological and Molecular Plant Pathology 62, 253-263. 

Decognet, V., and Nicot, P. (1999). Effects of fungicides on a Fusarium sp. biological control agent of Botrytis cinerea stem infections in the perspective of an integrated management of fungal diseases in 

greenhouse tomatoes. Bulletin OILB/SROP 22, 49-52. 

Decognet, V., Trottin-Caudal, Y., Fournier, C., Leyre, J. M., and Nicot, P. (1999). Protection of stem wounds against Botrytis cinerea in heated tomato greenhouses with a strain of Fusarium sp. Bulletin 

OILB/SROP 22, 53-56. 

Diaz, A., Poveda, D. C., and Cotes, A. M. (2007). Selection of crude fungal extracts with potential of control of Botrytis cinerea in tomato (Lycopersicon esculentum Mill.). Bulletin OILB/SROP 30, 49-53. 

Diaz, N. C., Barrera, M. J., and Granada, E. G. d. (1999). Controlling Botrytis cinerea Pers. in statice (Limonium sinuatum Mill.) 'Midnight Blue' cultivar. Acta Horticulturae, 235-238. 

86

Appendix 1 

Dik, A., and Wubben, J. (2001). Biological control of Botrytis cinerea in greenhouse crops. Bulletin OILB/SROP 24, 49-52. 

Dik, A. J., and Elad, Y. (1999). Comparison of antagonists of Botrytis cinerea in greenhouse-grown cucumber and tomato under different climatic conditions. European Journal of Plant Pathology 105, 123- 

137. 

Dik, A. J., Koning, G., and Köhl, J. (1999). Evaluation of microbial antagonists for biological control of Botrytis cinerea stem infection in cucumber and tomato. European Journal of Plant Pathology 105, 

115-122. 

Ding, Z., Liu, F., and Mu, L. (2002). UV-induced resistant strains of Trichoderma harzianum to procymidone. Chinese Journal of Biological Control 18, 75-78. 

Droby, S., Wisniewski, M., El-Ghaouth, A., and Wilson, C. (2003). Influence of food additives on the control of postharvest rots of apple and peach and efficacy of the yeast-based biocontrol product Aspire. 


Duraisamy, S., Ciavorella, A., Spadaro, D., Garibaldi, A., and Gullino, M. L. (2008). Metschnikowia pulcherrima strain MACH1 outcompetes Botrytis cinerea, Alternaria alternata and Penicillium expansum 

in apples through iron depletion. Postharvest Biology and Technology 49, 121-128. 

Edwards, S. G., and Seddon, B. (2001). Mode of antagonism of Brevibacillus brevis against Botrytis cinerea in vitro. Journal of Applied Microbiology 91, 652-659. 

El-Ghaouth, A., Smilanick, J. L., Brown, G. E., Ippolito, A., and Wilson, C. L. (2001a). Control of decay of apple and citrus fruits in semicommercial tests with Candida saitoana and 2-deoxy-D-glucose. 

Biological Control 20, 96-101. 

El-Ghaouth, A., Smilanick, J. L., and Wilson, C. L. (2000a). Enhancement of the performance of Candida saitoana by the addition of glycolchitosan for the control of postharvest decay of apple and citrus 

fruit. Postharvest Biology and Technology 19, 103-110. 

El-Ghaouth, A., Smilanick, J. L., Wisniewski, M., and Wilson, C. L. (2000b). Improved control of apple and citrus fruit decay with a combination of Candida saitoana and 2-deoxy-D-glucose. Plant Disease 

84, 249-253. 

El-Ghaouth, A., Wilson, C., and Wisniewski, M. (2001b). Evaluation of two biocontrol products, Bio-Coat and Biocure, for the control of postharvest decay of pome and citrus fruit. Bulletin OILB/SROP 24, 

161-165. 

El-Ghaouth, A., Wilson, C., and Wisniewski, M. (2001c). Induction of systemic resistance in apple by the yeast antagonist Candida saitoana. Bulletin OILB/SROP 24, 309-312. 

El-Neshawy, S., Osman, N., and Okasha, K. (1999). Biological control of neck rot and black mould of onion. Egyptian Journal of Agricultural Research 77, 125-137. 

El-Neshawy, S. M., and El-Morsy, F. M. (2003). Control of gray mold of grape by pre-harvest application of Candida oleophila and its combination with a low dosage of Euparen. Acta Horticulturae, 95-102. 

El-Neshawy, S. M., and Shetaia, Y. M. H. (2003). Biocontrol capability of Candida spp. against Botrytis rot of strawberries with respect to fruit quality. Acta Horticulturae, 727-733. 

El-Sheikh Aly, M. M., Baraka, M. A., and El-Sayed Abbass, A. G. (2000). The effectiveness of fumigants and biological protection of peach against fruit rots. Assiut Journal of Agricultural Sciences 31, 19- 

31. 

El-Zayat, S. A. (2008). Antimicrobial activities of secondary metabolites produced by endophytic fungi from Glinus lotoides. World Journal of Agricultural Sciences 4, 206-212. 

Elad, Y. (2000a). Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Protection 19, 709-714. 

Elad, Y. (2000b). Trichoderma harzianum T39 preparation for biocontrol of plant diseases - control of Botrytis cinerea, Sclerotinia sclerotiorum and Cladosporium fulvum. Biocontrol Science and Technology 

10, 499-507. 

Elad, Y., Baker, S. C., Faull, J. L., and Taylor, J. (2004). Multi trophic relationships - interaction of a biocontrol agent and a pathogen with the indigenous micro-flora on bean leaves. Bulletin OILB/SROP 27, 

151-154. 

Elad, Y., Kirshner, B., Yehuda, N., and Sztejnberg, A. (1998). Management of powdery mildew and gray mould of cucumber by Trichoderma harzianum T39 and Ampelomyces quisqualis AQ10. BioControl 

43, 241-251. 

Elmer, P. A. G., and Köhl, J. (1998). The survival and saprophytic competitive ability of the Botrytis spp. antagonist Ulocladium atrum in lily canopies. European Journal of Plant Pathology 104, 435-447. 

Enya, J., Shinohara, H., Yoshida, S., Tsukiboshi, T., Negishi, H., Suyama, K., and Tsushima, S. (2007). Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents. 

Microbial Ecology 53, 524-536. 

Essghaier, B., Sadfi-Zouaoui, N., Fardeau, M. L., Boudabous, A., Ollivier, B., Friel, D., and Jijakli, M. H. (2007). Post-harvest biological control of grey mould rot on strawberry fruits using moderately 

halophilic bacteria. Bulletin OILB/SROP 30, 73. 

Eva, B. (2003). Biological control of pathogens Sclerotinia sclerotiorum (Lib.) de Bary and Botrytis cinerea (Pers.) from sunflower (Helianthus annuus L.) crops. Cercetari Agronomice in Moldova 36, 73-80. 

Fan, Q., and Tian, S. (2001). Postharvest biological control of grey mold and blue mold on apple by Cryptococcus albidus (Saito) Skinner. Postharvest Biology and Technology 21, 341-350. 

Fan, Q., Tian, S., Jiang, A., and Xu, Y. (2001a). Isolation and screening of biocontrol antagonists of diseases of postharvest fruits. China Environmental Science 21, 313-316. 

Fan, Q., Tian, S., and Xu, Y. (2001b). Effects of Trichosporon sp. on biocontrol efficacy of grey and blue mold on postharvest apple. Scientia Agricultura Sinica 34, 163-168. 

Farrag, A. A. (2003). New approaches in biological control of Alternaria alternata and Botrytis cinerea attacking cucumber plants. African Journal of Mycology and Biotechnology 11, 189-205. 

Faten, S. M. (2005). Postharvest treatments of apple fruits decay caused by Botrytis cinerea, Alternaria alternata and Penicillium expansum. Annals of Agricultural Science (Cairo) 50, 613-633. 

87


Feng, S., Wang, R., Lin, K., Zhang, Y., Du, L., Fan, X., and Cao, W. (2003). Identification of strain Bs-208 and its inhibition against plant pathogenic fungi. Chinese Journal of Biological Control 19, 171-174. 

Fenice, M., and Gooday, G. W. (2006). Mycoparasitic actions against fungi and oomycetes by a strain (CCFEE 5003) of the fungus Lecanicillium muscarium isolated in Continental Antarctica. Annals of 

Microbiology 56, 1-6. 

Ferrari, A., Sicher, C., Prodorutti, D., and Pertot, I. (2007). Potential new applications of Shemer, a Metschnikowia fructicola based product, in post-harvest soft fruit rots control. Bulletin OILB/SROP 30, 43- 

46. 

Fiddaman, P. J., O'Neill, T. M., and Rossall, S. (2000). Screening of bacteria for the suppression of Botrytis cinerea and Rhizoctonia solani on lettuce (Lactuca sativa) using leaf disc bioassays. Annals of 

Applied Biology 137, 223-235. 

Filonow, A. B. (1998). Role of competition for sugars by yeasts in the biocontrol of gray mold of apple. Biocontrol Science and Technology 8, 243-256. 

Filonow, A. B., Vishniac, H. S., Anderson, J. A., and Janisiewicz, W. J. (1996). Biological control of Botrytis cinerea in apple by yeasts from various habitats and their putative mechanisms of antagonism. 


Fiume, F., and Fiume, G. (2005). Biological control of Botrytis Gray Mould and Sclerotinia Drop in lettuce. Communications in Agricultural and Applied Biological Sciences 70, 157-168. 

Fiume, G., Napolitano, S., Marziano, F., Ciscognetti, E., Correale, F., Raimo, S., Bove, C., and Fiume, F. (2008). Study of the antagonist fungus Trichoderma harzianum for the control of some tomato 

diseases. In "Giornate Fitopatologiche 2008, Cervia", pp. 547-554. 

Floch, G. l., Rey, P., Renault, A. S., Silue, D., Benhamou, N., and Tirilly, Y. (2001). Pythium oligandrum-mediated induced resistance against grey mould of tomato is associated with pathogenesis-related 

proteins. Bulletin OILB/SROP 24, 287-290. 

Floros, J. D., Dock, L. L., and Nielsen, P. V. (1998). Biological control of Botrytis cinerea growth on apples stored under modified atmospheres. Journal of Food Protection 61, 1661-1665. 

Fogliano, V., Ballio, A., Gallo, M., Woo, S., Scala, F., and Lorito, M. (2002). Pseudomonas lipodepsipeptides and fungal cell wall-degrading enzymes act synergistically in biological control. Molecular Plant- 

Microbe Interactions 15, 323-333. 

Fortes, F. d. O., Silva, A. C. F. d., Almanca, M. A. K., and Tedesco, S. B. (2007). Root induction from microcutting of an Eucalyptus sp. clone by Trichoderma spp. Revista Arvore 31, 221-228. 

Fowler, S. R., Jasper, M. V., Walter, M., and Stewart, A. (1999). Suppression of overwintering Botrytis cinerea inoculum on grape rachii using antagonistic fungi. Proceedings of the Fifty Second New 

Zealand Plant Protection Conference, Auckland Airport Centra, Auckland, New Zealand, 10-12 August, 1999, 141-147. 

Frankowski, J., Berg, G., and Bahl, H. (2001a). Purification and properties of two chitinolytic enzymes of the biocontrol agent Serratia plymuthica C48. Bulletin OILB/SROP 24, 319. 

Frankowski, J., Lorito, M., Scala, F., Schmid, R., Berg, G., and Bahl, H. (2001b). Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Archives of Microbiology 176, 421- 

426. 

Freeman, S., Barbul, O., David, D. R., Nitzani, Y., Zveibil, A., and Elad, Y. (2001). Trichoderma spp. for biocontrol of Colletotrichum acutatum and Botrytis cinerea in strawberry. Bulletin OILB/SROP 24, 

147-150. 

Freeman, S., Kolesnik, I., Barbul, O., Zveibil, A., Maymon, M., Nitzani, Y., Kirshner, B., Rav-David, D., and Elad, Y. (2002). Use of Trichoderma spp. for biocontrol of Colletotrichum acutatum 

(anthracnose) and Botrytis cinerea (grey mould) in strawberry, and study of biocontrol population survival by PCR. Bulletin OILB/SROP 25, 167-170. 

Freeman, S., Minz, D., Kolesnik, I., Barbul, O., Zveibil, A., Maymon, M., Nitzani, Y., Kirshner, B., Rav-David, D., Bilu, A., Dag, A., Shafir, S., and Elad, Y. (2004). Trichoderma biocontrol of Colletotrichum 

acutatum and Botrytis cinerea and survival in strawberry. European Journal of Plant Pathology 110, 361-370. 

Friel, D., and Jijakli, M. H. (2007). Simultaneous disruption of two exo- beta -1,3-glucanase genes of Pichia anomala significantly reduced the biological control efficiency against Botrytis cinerea and 

Penicillium expansum on apples. Bulletin OILB/SROP 30, 147. 

Friel, D., Pessoa, N. M. G., Vandenbol, M., and Jijakli, M. H. (2007). Separate and combined disruptions of two exo- beta -1,3-glucanase genes decrease the efficiency of Pichia anomala (strain K) biocontrol 

against Botrytis cinerea on apple. Molecular Plant-Microbe Interactions 20, 371-379. 

Fruit, L., and Nicot, P. (1999). Biological control of Botrytis cinerea on tomato stem wounds with Ulocladium atrum. Bulletin OILB/SROP 22, 81-84. 

Funaro, M. (1997). Importance and spread of techniques of integrated control in strawberry crops in Calabria. Informatore Agrario 53, 43-48. 

Gabler, F. M., Fassel, R., Mercier, J., and Smilanick, J. L. (2006). Influence of temperature, inoculation interval, and dosage on biofumigation with Muscodor albus to control postharvest gray mold on grapes. 

Plant Disease 90, 1019-1025. 

Gengotti, S., Ceredi, G., and Paoli, E. d. (2002). Anti-botrytis measures in organic and integrated strawberries. Informatore Agrario 58, 55-58. 

Gengotti, S., Ceredi, G., Paoli, E. d., and Antoniacci, L. (2000). Products and control strategies against strawberry grey mould in Emilia-Romagna. In "Atti, Giornate fitopatologiche, Perugia, 16-20 aprile, 

2000, Volume 2", pp. 299-304. 

Georgieva, O. (2004). Possibilities for biological control of gray mold of tomatoes (Botrytis cinerea) in view of the organotropic pathogen specialization. Ecology and Future - Bulgarian Journal of Ecological 

Science 3, 31-34. 

88

Appendix 1 

Gerlagh, M., Amsing, J. J., Molhoek, W. M. L., Bosker-van Zessen, A. I., Lombaers-van der Plas, C. H., and Köhl, J. (2001). The effect of treatment with Ulocladium atrum on Botrytis cinerea-attack of 

geranium (Pelargonium zonale) stock plants and cuttings. European Journal of Plant Pathology 107, 377-386. 

German Garcia, P., Jimenez, Y., Neisa, A., and Marina Cotes, A. (2001). Selection of native yeasts for biological control of postharvest rots caused by Botrytis allii in onion and Rhizopus stolonifer in tomato. 

Bulletin OILB/SROP 24, 181-184. 

Gielen, S., Aerts, R., and Seels, B. (2004a). Biocontrol agents of Botrytis cinerea tested in climate chambers by making artificial infection on tomato leafs. Communications in Agricultural and Applied 

Biological Sciences 69, 631-639. 

Gielen, S., Aerts, R., and Seels, B. (2004b). Different products for biological control of Botrytis cinerea examined on wounded stem tissue of tomato plants. Communications in Agricultural and Applied 


Giraud, M., and Crouzet, M. P. (2004). Control of storage diseases of apples and pears. A yeast for biological protection. Results of three years of European tests. Infos-Ctifl, 38-40. 

Grevesse, C., Lepoivre, P., and Mohamed Haissam, J. (2003). Characterization of the exoglucanase-encoding gene PaEXG2 and study of its role in the biocontrol activity of Pichia anomala strain K. 

Phytopathology 93, 1145-1152. 

Gromovikh, T. I., Gukasian, V. M., Golovanova, T. I., and Shmarlovskaya, S. V. (1998). Trichoderma harzianum Rifai Aggr. as a factor enhancing tomato plants resistance to the root rotting pathogens. 

Mikologiya i Fitopatologiya 32, 73-78. 

Gu, Z., Chen, W., Cheng, H., Ma, C., Gong, X., and Shen, L. (2008). Improvement of antifungal activity of Bacillus subtilis G3 by mutagenesis with acridine orange. Acta Phytopathologica Sinica 38, 185- 

191. 

Gu, Z., Ma, C., and Han, C. a. (2001). Inhibitory action of chitinase producing Bacillus spp. to pathogenic fungi. Acta Agriculturae Shanghai 17, 88-92. 

Gu, Z., Wu, W., Gao, X., and Ma, C. (2004). Antifungal substances of Bacillus subtilis strain G3 and their properties. Acta Phytopathologica Sinica 34, 166-172. 

Guetsky, R., Elad, Y., Shtienberg, D., and Dinoor, A. (2002a). Establishment, survival and activity of the biocontrol agents Pichia guillermondii and Bacillus mycoides applied as a mixture on strawberry 

plants. Biocontrol Science and Technology 12, 705-714. 

Guetsky, R., Elad, Y., Shtienberg, D., and Dinoor, A. (2002b). Improved biocontrol of Botrytis cinerea on detached strawberry leaves by adding nutritional supplements to a mixture of Pichia guilermondii and 

Bacillus mycoides. Biocontrol Science and Technology 12, 625-630. 

Guetsky, R., Shtienberg, D., Elad, Y., and Dinoor, A. (2001a). Combining biocontrol agents to reduce the variability of biological control. Phytopathology 91, 621-627. 

Guetsky, R., Shtienberg, D., Elad, Y., and Dinoor, A. (2001b). Establishment, survival and activity of biocontrol agents applied as a mixture in strawberry crops. Bulletin OILB/SROP 24, 193-196. 

Guinebretiere, M. H., Nguyen-The, C., Morrison, N., Reich, M., and Nicot, P. (2000). Isolation and characterization of antagonists for the biocontrol of the postharvest wound pathogen Botrytis cinerea on 

strawberry fruits. Journal of Food Protection 63, 386-394. 

Gulati, M. K., Koch, E., and Zeller, W. (1999). Isolation and identification of antifungal metabolites produced by fluorescent Pseudomonas, antagonist of red core disease of strawberry. In "Modern fungicides 

and antifungal compounds II. 12th International Reinhardsbrunn Symposium, Friedrichroda, Thuringia, Germany, 24th-29th May 1998." pp. 437-444. 

Guo, Y., Zheng, H., Yang, Y., and Wang, H. (2007). Characterization of Pseudomonas corrugata strain P94 isolated from soil in Beijing as a potential biocontrol agent. Current Microbiology 55, 247-253. 

Guven, K., Ilhan, S., Mutlu, M. B., and Colak, F. (2008). Diversity, characterization and antimicrobial activities of Bacillus cereus strains isolated from soil. Fresenius Environmental Bulletin 17, 303-310. 

Halama, P., and Haluwin, C. v. (2004). Antifungal activity of lichen extracts and lichenic acids. BioControl 49, 95-107. 

Han, S., Xu, M., Bai, Z., Wu, W., and Lu, A. (2004). Studies on the antibiotic from actinomyces D2-4 against fungal disease. Journal of Microbiology 24, 8-10. 

Harman, G. E., Latorre, B., Agosin, E., Martin, R. s., Riegel, D. G., Nielsen, P. A., Tronsmo, A., and Pearson, R. C. (1996). Biological and integrated control of Botrytis bunch rot of grape using Trichoderma 

spp. Biological Control 7, 259-266. 

Helbig, J. (2001a). Biological control of Botrytis cinerea Pers. ex Fr. in strawberry by Paenibacillus polymyxa (isolate 18191). Journal of Phytopathology 149, 265-273. 

Helbig, J. (2001b). Field and laboratory investigations into the effectiveness of Rhodotorula glutinis (isolate 10391) against Botrytis cinerea Pers. ex Fr. in strawberry. Zeitschrift fur Pflanzenkrankheiten und 

Pflanzenschutz 108, 356-368. 

Helbig, J. (2002). Ability of the antagonistic yeast Cryptococcus albidus to control Botrytis cinerea in strawberry. BioControl 47, 85-99. 

Helbig, J., and Bochow, H. (2001). Effectiveness of Bacillus subtilis (isolate 25021) in controlling Botrytis cinerea in strawberry. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz 108, 545-559. 

Helbig, J., Trierweiler, B., Schutz, F. A., and Tauscher, B. (1998). Inhibition of Botrytis cinerea pers. ex Fr. and Penicillium digitatum Sacc. by Bacillus sp. (isolate 17141) in vitro. Zeitschrift fur 

Pflanzenkrankheiten und Pflanzenschutz 105, 8-16. 

Hernandez-Rodriguez, A., Hernandez-Lauzardo, A. N., Velazquez-del Valle, M. G., Bigiramana, Y., Audenaert, K., and Hofte, M. (2004). Use of rhizobacteria to induce resistance in bean (Phaseolus vulgaris 

L.) infected by Colletotrichum lindemuthianum (Sacc. and Magnus) Lams.-Scrib. and in tomato (Lycopersicon esculentum Mill.) infected by Botrytis cinerea Pers.:Fr. Revista Mexicana de Fitopatologia 

22, 100-106. 

89


Hjeljord, L. G. (2002). Conidial germination initiation in the fungal antagonist Trichoderma harzianum (atroviride) P1 in the context of biological control of plant disease. In "Conidial germination initiation in 

the fungal antagonist Trichoderma harzianum", pp. 30 pp. + appendices. 

Hjeljord, L. G., Stensvand, A., and Tronsmo, A. (2000). Effect of temperature and nutrient stress on the capacity of commercial Trichoderma products to control Botrytis cinerea and Mucor piriformis in 

greenhouse strawberries. Biological Control 19, 149-160. 

Hjeljord, L. G., Stensvand, A., and Tronsmo, A. (2001). Antagonism of nutrient-activated conidia of Trichoderma harzianum (atroviride) P1 against Botrytis cinerea. Phytopathology 91, 1172-1180. 

Hjeljord, L. G., and Tronsmo, A. (2003). Effect of germination initiation on competitive capacity of Trichoderma atroviride P1 conidia. Phytopathology 93, 1593-1598. 

Hmouni, A., Massoui, M., and Douira, A. M. (1999). Study of antagonistic activity of Trichoderma spp. and Gliocladium spp. against Botrytis cinerea: causal agent of tomato grey mould. Al Awamia, 75-92. 

Hmouni, A., Mouria, A., and Douira, A. (2005). Study of the receptivity of tomato leaves to Botrytis cinerea, causal agent of grey mould in relation to the biocontrol activities of Trichoderma and Gliocladium. 

Al Awamia, 31-48. 

Hmouni, A., Mouria, A., and Douira, A. (2006). Biological control of tomato grey mould with compost water extracts, Trichoderma species and Gliocladium species. Phytopathologia Mediterranea 45, 110- 

116. 

Holmes, R. J., Alwis, S. d., Shanmuganathan, N., Widyatuti, S., and Keane, P. J. (1998). Enhanced biocontrol of postharvest diseases of apples and pears. ACIAR Proceedings Series, 162-166. 

Holz, G., and Volkmann, A. (2002). Colonisation of different positions in grape bunches by potential biocontrol organisms and subsequent occurrence of Botrytis cinerea. Bulletin OILB/SROP 25, 9-12. 

Honda, N., Hirai, M., Ano, T., and Shoda, M. (1999). Control of tomato damping-off caused by Rhizoctonia solani by the heterotrophic nitrifier Alcaligenes faecalis and its product, hydroxylamine. Annals of 

the Phytopathological Society of Japan 65, 153-162. 

Horst, L. E., Locke, J., Krause, C. R., McMahon, R. W., Madden, L. V., and Hoitink, H. A. J. (2005). Suppression of Botrytis blight of begonia by Trichoderma hamatum 382 in peat and compost-amended 

potting mixes. Plant Disease 89, 1195-1200. 

Hsieh, F. C., Li, M. C., and Kao, S. S. (2003). Evaluation of the inhibition activity of Bacillus subtilis-based products and their related metabolites against pathogenic fungi in Taiwan. Plant Protection Bulletin 

(Taipei) 45, 155-162. 

Hsieh, F. C., Lin, T. C., Tseng, J. T., and Kao, S. S. (2004). An entomopathogenic-nematophilic bacterium, Photorhabdus luminescens, with insecticidal and antimicrobial activities. Plant Protection Bulletin 

(Taipei) 46, 163-172. 

Huang, C. J., and Chen, C. Y. (2004). Gene cloning and biochemical characterization of chitinase CH from Bacillus cereus 28-9. Annals of Microbiology 54, 289-297. 

Huang, H., and Erickson, R. S. (2002). Biological control of botrytis stem and blossom blight of lentil. Plant Pathology Bulletin 11, 7-14. 

Huang, H., and Erickson, R. S. (2005). Control of lentil seedling blight caused by Botrytis cinerea using microbial seed treatments. Plant Pathology Bulletin 14, 35-40. 

Indiragandhi, P., Anandham, R., Madhaiyan, M., and Sa, T. M. (2008). Characterization of plant growth-promoting traits of bacteria isolated from larval guts of Diamondback moth Plutella xylostella 

(Lepidoptera: Plutellidae). Current Microbiology 56, 327-333. 

Ingram, D. M., and Meister, C. W. (2006). Managing Botrytis gray mold in greenhouse tomatoes using traditional and bio-fungicides. Plant Health Progress, 1-5. 

Ippolito, A., Schena, L., Pentimone, I., and Nigro, F. (2005a). Control of postharvest rots of sweet cherries by pre- and postharvest applications of Aureobasidium pullulans in combination with calcium 

chloride or sodium bicarbonate. Postharvest Biology and Technology 36, 245-252. 

Ippolito, A., Schena, L., Pentimone, I., and Nigro, F. (2005b). Integrated control of sweet cherry postharvest rots by Aureobasidium pullulans in combination with calcium chloride or sodium bicarbonate. Acta 

Horticulturae, 1985-1990. 

Jackson, A. J., Walters, D. R., and Marshall, G. (1997). Antagonistic interactions between the foliar pathogen Botrytis fabae and isolates of Penicillium brevicompactum and Cladosporium cladosporioides on 

faba beans. Biological Control 8, 97-106. 

Jalil R, C., Norero S, A., and Apablaza H, G. (1997). Effects of temperature on mycelial growth of Botrytis cinerea and its antagonist Trichoderma harzianum. Ciencia e Investigacion Agraria 24, 125-132. 

Jamalizadeh, M., Etebarian, H. R., Alizadeh, A., and Aminian, H. (2008). Biological control of gray mold on apple fruits by Bacillus licheniformis (EN74-1). Phytoparasitica 36, 23-29. 

Janisiewicz, W. J., and Jeffers, S. N. (1997). Efficacy of commercial formulation of two biofungicides for control of blue mold and gray mold of apples in cold storage. Crop Protection 16, 629-633. 

Jaworska, M., and Dluzniewska, J. (2007). The effect of manganese ions on development and antagonism of Trichoderma isolates. Polish Journal of Environmental Studies 16, 549-553. 

Ji, Z., Tang, L., Zhang, Q., Xu, J., Chen, X., and Tong, Y. (2007). Isolation, purification and characterization of antifungal protein from Bacillus licheniformis W10 strain. Acta Phytopathologica Sinica 37, 

260-264. 

Jijakli, H., Lassois, L., and Lahlali, R. (2004). Antagonistic activity of yeast against post-harvest diseases of tropical fruits. Bulletin des Seances, Academie Royale des Sciences d'Outre- Mer 50, 153-163. 

Jijakli, M. H. (2000). Apples: storage diseases. Biological control based on two yeast strains. Arboriculture Fruitiere, 19-23. 

Jijakli, M. H., Clercq, D. d., Dickburt, C., and Lepoivre, P. (2002). Pre- and post-harvest practical application of Pichia anomala strain K, beta -1,3-glucans and calcium chloride on apples: two years of 

monitoring and efficacy against post-harvest diseases. Bulletin OILB/SROP 25, 29-32. 

Jijakli, M. H., and Lepoivre, P. (1998). Characterization of an exo- beta -1,3-glucanase produced by Pichia anomala strain K, antagonist of Botrytis cinerea on apples. Phytopathology 88, 335-343. 

90

Appendix 1 

Jing, W., Tu, K., Shao, X., and Su, Z. (2008). Effects of combinations of hot water rinsing and brushing and yeast antagonist for control of decay and quality on harvested sweet cherries. Journal of Fruit 

Science 25, 367-372. 

Kalogiannis, S., Tjamos, S. E., Stergiou, A., Antoniou, P. P., Ziogas, B. N., and Tjamos, E. C. (2006). Selection and evaluation of phyllosphere yeasts as biocontrol agents against grey mould of tomato. 

European Journal of Plant Pathology 116, 69-76. 

Kamensky, M., Ovadis, M., Chet, I., and Chernin, L. (2002). Biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum in the greenhouse by a Serratia plymuthica strain with multiple mechanisms of 

antifungal activity. Bulletin OILB/SROP 25, 229-232. 

Kamensky, M., Ovadis, M., Chet, I., and Chernin, L. (2003). Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and 

Sclerotinia sclerotiorum diseases. Soil Biology & Biochemistry 35, 323-331. 

Kandybin, N. V. (2003). For activization of microbiomethod. Zashchita i Karantin Rastenii, 13-14. 

Kapat, A., Zimand, G., and Elad, Y. (1998). Effect of two isolates of Trichoderma harzianum on the activity of hydrolytic enzymes produced by Botrytis cinerea. Physiological and Molecular Plant Pathology 

52, 127-137. 

Karabulut, O. A., Arslan, U., Ilhan, K., and Kuruoglu, G. (2005). Integrated control of postharvest diseases of sweet cherry with yeast antagonists and sodium bicarbonate applications within a hydrocooler. 


Karabulut, O. A., and Baykal, N. (2003). Biological control of postharvest diseases of peaches and nectarines by yeasts. Journal of Phytopathology 151, 130-134. 

Karabulut, O. A., and Baykal, N. (2004). Integrated control of postharvest diseases of peaches with a yeast antagonist, hot water and modified atmosphere packaging. Crop Protection 23, 431-435. 

Karabulut, O. A., Smilanick, J. L., Gabler, F. M., Mansour, M., and Droby, S. (2003). Near-harvest applications of Metschnikowia fructicola, ethanol, and sodium bicarbonate to control postharvest diseases of 

grape in central California. Plant Disease 87, 1384-1389. 

Karabulut, O. A., Tezcan, H., Daus, A., Cohen, L., Wiess, B., and Droby, S. (2004). Control of preharvest and postharvest fruit rot in strawberry by Metschnikowia fructicola. Biocontrol Science and 


Kessel, G. (1999). Biological control of Botrytis spp. by Ulocladium atrum: an ecological analysis. In "Biological control of Botrytis spp. by Ulocladium atrum: an ecological analysis." pp. 155 pp. 

Kessel, G. J. T., Haas, B. H. d., Lombaers-van der Plas, C. H., Ende, J. E. v. d., Pennock-Vos, M. G., Werf, W. v. d., and Köhl, J. (2001). Comparative analysis of the role of substrate specificity in biological 

control of Botrytis elliptica in lily and B. cinerea in cyclamen with Ulocladium atrum. European Journal of Plant Pathology 107, 273-284. 

Kessel, G. J. T., Haas, B. H. d., Lombaers-van der Plas, C. H., Meijer, E. M. J., Dewey, F. M., Goudriaan, J., Werf, W. v. d., and Köhl, J. (1999). Quantification of mycelium of Botrytis spp. and the antagonist 

Ulocladium atrum in necrotic leaf tissue of cyclamen and lily by fluorescence microscopy and image analysis. Phytopathology 89, 868-876. 

Kessel, G. J. T., Haas, B. H. d., Werf, W. v. d., and Köhl, J. (2002). Competitive substrate colonisation by Botrytis cinerea and Ulocladium atrum in relation to biological control of B. cinerea in cyclamen. 

Mycological Research 106, 716-728. 

Kessel, G. J. T., Köhl, J., Powell, J. A., Rabbinge, R., and Werf, W. v. d. (2005). Modeling spatial characteristics in the biological control of fungi at leaf scale: competitive substrate colonization by Botrytis 

cinerea and the saprophytic antagonist Ulocladium atrum. Phytopathology 95, 439-448. 

Khan, M. S., and Almas, Z. (2002). Plant growth promoting rhizobacteria from rhizospheres of wheat and chickpea. Annals of Plant Protection Sciences 10, 265-271. 

Khan, M. S., Almas, Z., and Wani, P. A. (2006). Determination of antagonistic potentials of Azotobacter to fungal phytopathogens. Annals of Plant Protection Sciences 14, 492-494. 

Kim, B., Moon, S., and Hwang, B. (1999). Isolation, antifungal activity, and structure elucidation of the glutarimide antibiotic, streptimidone, produced by Micromonospora coerulea. Journal of Agricultural 

and Food Chemistry 47, 3372-3380. 

Kim, J., Choi, G., Kim, H., Kim, H., Ahn, J., and Cho, K. (2002). Verlamelin, an antifungal compound produced by a mycoparasite, Acremonium strictum. Plant Pathology Journal 18, 102-105. 

Kim, K., Kang, J., Moon, S., and Kang, K. (2000). Isolation and identification of antifungal N-butylbenzenesulphonamide produced by Pseudomonas sp. AB2. Journal of Antibiotics 53, 131-136. 

Kim, P. I., Bai, H., Bai, D., Chae, H., Chung, S., Kim, Y., Park, R., and Chi, Y. T. (2004). Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. Journal of Applied 


Kim, S., Yoo, S., and Kim, H. (1997). Selection of antagonistic bacteria for biological control of ginseng diseases. Korean Journal of Plant Pathology 13, 342-348. 

Kim, Y., Kim, H., Chang, C., Hwang, I., Oh, H., Ahn, J., Kim, K., Hwang, B., and Kim, B. (2007). Biological evaluation of neopeptins isolated from a Streptomyces strain. Pest Management Science 63, 

1208-1214. 

Kishore, G. K., and Pande, S. (2007). Chitin-supplemented foliar application of chitinolytic Bacillus cereus reduces severity of Botrytis gray mold disease in chickpea under controlled conditions. Letters in 

Applied Microbiology 44, 98-105. 

Klemsdal, S. S., Clarke, J. L., Hoell, I. A., Eijsink, V. G. H., and Brurberg, M. B. (2006). Molecular cloning, characterization, and expression studies of a novel chitinase gene (ech30) from the mycoparasite 

Trichoderma atroviride strain P1. FEMS Microbiology Letters 256, 282-289. 

Köhl, J., Evenhuis, B., and Boff, P. (2004). Integration of the use of the antagonist Ulocladium atrum in management of strawberry grey mould (Botrytis cinerea). Bulletin OILB/SROP 27, 95-98. 

91


Köhl, J., and Fokkema, N. J. (1998). Biological control of Botrytis cinerea by suppression of sporulation. In "Brighton Crop Protection Conference: Pests & Diseases - 1998: Volume 2: Proceedings of an 

International Conference, Brighton, UK, 16-19 November 1998." pp. 681-692. 

Köhl, J., and Gerlagh, M. (1999). Biological control of Botrytis cinerea in roses by the antagonist Ulocladium atrum. Mededelingen - Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, 

Universiteit Gent 64, 441-445. 

Köhl, J., Gerlagh, M., and Grit, G. (2000). Biocontrol of Botrytis cinerea by Ulocladium atrum in different production systems of cyclamen. Plant Disease 84, 569-573. 

Köhl, J., Gerlagh, M., Haas, B. H. d., and Krijger, M. C. (1998). Biological control of Botrytis cinerea in cyclamen with Ulocladium atrum and Gliocladium roseum under commercial growing conditions. 


Köhl, J., Kessel, G. J. T., Boff, P., Kraker, J. d., and Werf, W. v. d. (2001). Epidemiology of Botrytis spp. in different crops determines success of biocontrol by competitive substrate exclusion by Ulocladium 

atrum. Bulletin OILB/SROP 24, 171-174. 

Köhl, J., and Molhoek, W. M. L. (2001). Effect of water potential on conidial germination and antagonism of Ulocladium atrum against Botrytis cinerea. Phytopathology 91, 485-491. 

Köhl, J., Molhoek, W. W. L., Goossen-van de Geijn, H. M., and Lombaers-van der Plas, C. H. (2003). Potential of Ulocladium atrum for biocontrol of onion leaf spot through suppression of sporulation of 

Botrytis spp. BioControl 48, 349-359. 

Köhl, J., Plas, C. H. L. v. d., Molhoek, W. M. L., Kessel, G. J. T., and Geijn, H. M. G. v. d. (1999). Competitive ability of the antagonists Ulocladium atrum and Gliocladium roseum at temperatures favourable 

for Botrytis spp. development. BioControl 44, 329-346. 

Koike, M., Higashio, T., Komori, A., Akiyama, K., Kishimoto, N., Masuda, E., Sasaki, M., Yoshida, S., Tani, M., Kuramoti, K., Sugimoto, M., and Nagao, H. (2004). Verticillium lecanii (Lecanicillium spp.) 

as epiphyte and its application to biological control of arthropod pests and diseases. Bulletin OILB/SROP 27, 41-44. 

Konstantinidou-Doltsinis, S., Markellou, E., Petsikos-Panayotarou, N., Siranidou, E., Kalamarakis, A. E., Schmitt, A., Ernst, A., Seddon, B., Belanger, R. R., and Dik, A. J. (2002). Combinations of biocontrol 

agents and Milsana(R) against powdery mildew and grey mould in cucumber in Greece and the Netherlands. Bulletin OILB/SROP 25, 171-174. 

Kornilov, A. V., Sitnikov, A. V., and Smirnov, Y. V. (2007). Bakflor on tomatoes. Kartofel' i Ovoshchi, 24. 

Korolev, N., and Elad, Y. (2004). Systemic resistance in Arabidopsis thaliana induced by biocontrol agent Trichoderma harzianum. Bulletin OILB/SROP 27, 363-366. 

Kovach, J., Petzoldt, R., and Harman, G. E. (2000). Use of honey bees and bumble bees to disseminate Trichoderma harzianum 1295-22 to strawberries for Botrytis control. Biological Control 18, 235-242. 

Krol, E. (1998). Epiphytic bacteria isolated from grape leaves and its effect on Botrytis cinerea pers. Phytopathologia Polonica, 53-61. 

Kulakiotu, E., and Sfakiotakis, E. (2003a). Influence of inoculation time after wounding on the action of Isabella volatiles against Botrytis cinerea. Bulletin OILB/SROP 26, 71-74. 

Kulakiotu, E. K., and Sfakiotakis, E. M. (2003b). Influence of grape volatiles of Vitis labrusca 'Isabella' on growth of Botrytis cinerea on 'Hayward' kiwifruit. Acta Horticulturae, 445-446. 

Kulakiotu, E. K., Thanassoulopoulos, C. C., and Sfakiotakis, E. M. (2004a). Biological control of Botrytis cinerea by volatiles of 'Isabella' grapes. Phytopathology 94, 924-931. 

Kulakiotu, E. K., Thanassoulopoulos, C. C., and Sfakiotakis, E. M. (2004b). Postharvest biological control of Botrytis cinerea on kiwifruit by volatiles of "Isabella" grapes. Phytopathology 94, 1280-1285. 

Kumar, R. S., Ayyadurai, N., Pandiaraja, P., Reddy, A. V., Venkateswarlu, Y., Prakash, O., and Sakthivel, N. (2005). Characterization of antifungal metabolite produced by a new strain Pseudomonas 

aeruginosa PUPa3 that exhibits broad-spectrum antifungal activity and biofertilizing traits. Journal of Applied Microbiology 98, 145-154. 

Kuptsov, V., Kolomiets, E., and Sverchkova, N. (2004). Evaluation of antifungal activity of bacteria-antagonists towards lupin pathogens. In "Wild and cultivated lupins from the Tropics to the Poles. 

Proceedings of the 10th International Lupin Conference, Laugarvatn, Iceland, 19-24 June 2002", pp. 258-260. 

Kurtzman, C. P., and Droby, S. (2001). Metschnikowia fructicola, a new ascosporic yeast with potential for biocontrol of postharvest fruit rots. Systematic and Applied Microbiology 24, 395-399. 

Lahdenpera, M. L., and Korteniemi, M. (2008). Application methods for commercial biofungicides in greenhouses. Bulletin OILB/SROP 32, 111-114. 

Lahlali, R., Friel, D., and Jijakli, M. H. (2007). Comparative study of the ecological niche of Penicillum expansum Link., Botrytis cinerea Pers. and their antagonistic yeasts Candida oleophila strain O and 

Pichia anomala strain K. Bulletin OILB/SROP 30, 235-239. 

Lee, J., Bae, D., Park, S., Shim, C., Kwak, Y., and Kim, H. (2001). Occurrence and biological control of postharvest decay in onion caused by fungi. Plant Pathology Journal 17, 141-148. 

Lee, J., Lee, S., Kim, C., Son, J., Song, J., Lee, K., Kim, H., Jung, S., and Moon, B. (2006). Evaluation of formulations of Bacillus licheniformis for the biological control of tomato gray mold caused by 

Botrytis cinerea. Biological Control 37, 329-337. 

Leibinger, W., Breuker, B., Hahn, M., and Mendgen, K. (1997). Control of postharvest pathogens and colonization of the apple surface by antagonistic microorganisms in the field. Phytopathology 87, 1103- 

1110. 

Lennartz, B., Schoene, P., and Oerke, E. C. (1998). Biocontrol of Botrytis cinerea on grapevine and Septoria spp. on wheat. Mededelingen - Faculteit Landbouwkundige en Toegepaste Biologische 

Wetenschappen, Universiteit Gent 63, 963-970. 

Levy, N. O., Elad, Y., and Katan, J. (2004a). Integration of Trichoderma and soil solarization for disease management. Bulletin OILB/SROP 27, 65-70. 

Levy, N. O., Elad, Y., Katan, J., Baker, S. C., and Faull, J. L. (2006). Trichoderma and soil solarization induced microbial changes on plant surfaces. Bulletin OILB/SROP 29, 21-26. 

Levy, N. O., Elad, Y., Korolev, N., and Katan, J. (2004b). Resistance induced by soil biocontrol application and soil solarization for the control of foliar pathogens. Bulletin OILB/SROP 27, 171-176. 

92

Appendix 1 

Li, G. Q., Huang, H. C., Acharya, S. N., and Erickson, R. S. (2004a). Biological control of blossom blight of alfalfa caused by Botrytis cinerea under environmentally controlled and field conditions. Plant 

Disease 88, 1246-1251. 

Li, G. Q., Huang, H. C., Kokko, E. G., and Acharya, S. N. (2002). Ultrastructural study of mycoparasitism of Gliocladium roseum on Botrytis cinerea. Botanical Bulletin of Academia Sinica 43, 211-218. 

Li, H., White, D., Lamza, K. A., Berger, F., and Leifert, C. (1998). Biological control of Botrytis, Phytophthora and Pythium by Bacillus subtilis Cot1 and CL27 of micropropagated plants in high-humidity 

fogging glasshouses. Plant Cell, Tissue and Organ Culture 52, 109-112. 

Li, Y., Liu, S., Li, M., Zhao, J., Li, J., and Wen, M. (2008). Separation and identification of oligomycins A and C from Streptomyces luteogriseus ECO 00001 and their bioactive properties. Acta 

Phytophylacica Sinica 35, 47-50. 

Li, Z., He, Y., and Xia, X. (2004b). Inhibitory spectrum and partial biological traits of five Trichoderma isolates. Journal of Yunnan Agricultural University 19, 267-271. 

Li, Z., Xiang, J., Chen, J., Ge, C., and Ge, S. (2007). Isolation and identification of actinomycete against Fusarium graminearum Schw. Journal of Triticeae Crops 27, 149-152. 

Lian, C., Li, S., Chao, C., Ma, P., Jiang, J., and Lu, X. (2007). Selection, identification and characterization of antagonistic and phytohormone producing bacterial strain CX-5-2. Acta Phytopathologica Sinica 

37, 197-203. 

Liang, Y., Zong, Z., and Ma, Q. (2007). Inhibiting and promoting effect on plants of six strains endophytic actinomycetes isolated from wild plants. Journal of Northwest A & F University - Natural Science 

Edition 35, 131-136. 

Lima, G., Arru, S., Curtis, F. d., and Arras, G. (1999). Influence of antagonist, host fruit and pathogen on the biological control of postharvest fungal diseases by yeasts. Journal of Industrial Microbiology & 

Biotechnology 23, 223-229. 

Lima, G., Castoria, R., Spina, A. M., Curtis, F. d., and Caputo, L. (2005). Improvement of biocontrol yeast activity against postharvest pathogens: recent experiences. Acta Horticulturae, 2035-2040. 

Lima, G., Curtis, F. d., Castoria, R., and Cicco, V. d. (1998). Activity of the yeasts Cryptococcus laurentii and Rhodotorula glutinis against post-harvest rots on different fruits. Biocontrol Science and 


Lima, G., Curtis, F. d., Castoria, R., and Cicco, V. d. (2003). Integrated control of apple postharvest pathogens and survival of biocontrol yeasts in semi-commercial conditions. European Journal of Plant 

Pathology 109, 341-349. 

Lima, G., Curtis, F. d., Piedimonte, D., Spina, A. M., and Cicco, V. d. (2006). Integration of biological control yeast and thiabendazole protects stored apples from fungicide sensitive and resistant isolates of 

Botrytis cinerea. Postharvest Biology and Technology 40, 301-307. 

Lima, G., Ippolito, A., Nigro, F., and Salerno, M. (1997). Biological control of grey mould of stored table grapes by pre-harvest applications of Aureobasidium pullulans and Candida oleophila. Difesa delle 

Piante 20, 21-28. 

Limon, M. C., Chacon, M. R., Mejias, R., Delgado-Jarana, J., Rincon, A. M., Codon, A. C., and Benitez, T. (2004). Increased antifungal and chitinase specific activities of Trichoderma harzianum CECT 2413 

by addition of a cellulose binding domain. Applied Microbiology and Biotechnology 64, 675-685. 

Lisboa, B. B., Bochese, C. C., Vargas, L. K., Silveira, J. R. P., Radin, B., and Oliveira, A. M. R. d. (2007). Efficiency of Trichoderma harzianum and Gliocladium viride in decreasing the incidence of Botrytis 

cinerea in tomato cultivated in protected environment. Ciencia Rural 37, 1255-1260. 

Liu, B., Peng, H., and Chen, S. (2007a). Screening of Trichoderma antagonistic strains to Tomato Botrytis cinerea and its evaluation of the control effect. Southwest China Journal of Agricultural Sciences 20, 

650-653. 

Liu, C. H., Chen, X., Liu, T. T., Lian, B., Gu, Y., Caer, V., Xue, Y. R., and Wang, B. T. (2007b). Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its 

antifungal components. Applied Microbiology and Biotechnology 76, 459-466. 

Liu, Q., Yu, J., and Fang, S. (2004). Antagonism appraisement of strain MY02 against plant pathogenic fungus. Journal of Jilin Agricultural University 26, 499-502. 

Liu, X., Li, Q., Wang, Y., Xu, X., and Zhang, X. (2006). The antifungal activity of secondary metabolic products from Xenorhabdus nematophilus YL001. Acta Phytophylacica Sinica 33, 277-281. 

Liu, Y., Chen, Z., Ng, T. B., Zhang, J., Zhou, M., Song, F., Lu, F., and Liu, Y. (2007c). Bacisubin, an antifungal protein with ribonuclease and hemagglutinating activities from Bacillus subtilis strain B-916. 

Peptides 28, 553-559. 

Liu, Y., Huang, C., and Chen, C. (2008). Evidence of induced systemic resistance against Botrytis elliptica in lily. Phytopathology 98, 830-836. 

Lolas, M., Donoso, E., Gonzalez, V., and Carrasco, G. (2005). Use of a Chilean native strain 'Sherwood' of Trichoderma virens on the biocontrol of Botrytis cinerea in lettuces grown by a float system. Acta 


Long, J., Hu, Z., Liu, J., and Wu, W. (2005). Fungicidal activity of fermentation products of Streptomyces isolated from Qinling mountain area. Chinese Journal of Biological Control 21, 187-191. 

Ma, Y., Liu, X., Gao, K., Qin, N., Pang, Y., and Shi, C. (2007). Preliminary study on biocontrol potential of rhizobacterium Serratia plymuthica HRO-C48. Journal of Yunnan Agricultural University 22, 49- 

53. 

Maccagnani, B., Mocioni, M., Gullino, M. L., and Ladurner, E. (1999). Application of Trichoderma harzianum by using Apis mellifera as a vector for the control of grey mould of strawberry: first results. 


93


Mach, R. L., Peterbauer, C. K., Payer, K., Jaksits, S., Woo, S. L., Zeilinger, S., Kullnig, C. M., Lorito, M., and Kubicek, C. P. (1999). Expression of two major chitinase genes of Trichoderma atroviride (T. 

harzianum P1) is triggered by different regulatory signals. Applied and Environmental Microbiology 65, 1858-1863. 

Machowicz-Stefaniak, Z. (1998). Antagonistic activity of epiphytic fungi from grape-vine against Botrytis cinerea Pers. Phytopathologia Polonica, 45-52. 

Machowicz-Stefaniak, Z., Prischepa, L. I., Zalewska, E., and Krol, E. (2004). Effect of Trichoderma spp. on some pathogens of hazel. Annales Universitatis Mariae Curie-Sklodowska. Sectio EEE, 

Horticultura 14, 101-110. 

Magnin-Robert, M., Trotel-Aziz, P., Quantinet, D., Biagianti, S., and Aziz, A. (2007). Biological control of Botrytis cinerea by selected grapevine-associated bacteria and stimulation of chitinase and beta -1,3 

glucanase activities under field conditions. European Journal of Plant Pathology 118, 43-57. 

Mahmoud, Y. A. G., Ebrahim, M. K. H., and Aly, M. M. (2004). Influence of some plant extracts and microbioagents on some physiological traits of faba bean infected with Botrytis fabae. Turkish Journal of 

Botany 28, 519-528. 

Mamarabadi, M., Jensen, B., Jensen, D. F., and Lubeck, M. (2008). Real-time RT-PCR expression analysis of chitinase and endoglucanase genes in the three-way interaction between the biocontrol strain 

Clonostachys rosea IK726, Botrytis cinerea and strawberry. FEMS Microbiology Letters 285, 101-110. 

Marco, S. d., and Osti, F. (2007). Applications of Trichoderma to prevent Phaeomoniella chlamydospora infections in organic nurseries. Phytopathologia Mediterranea 46, 73-83. 

Mari, M., Guizzardi, M., and Pratella, G. C. (1996). Biological control of gray mold in pears by antagonistic bacteria. Biological Control 7, 30-37. 

Marquenie, D., Schenk, A., and Nicolai, B. (1999). VCBT investigates non-chemical methods to increase the storage life of strawberries and sweet cherries. Fruitteelt-nieuws 12, 18-19. 

Masih, E. I., Alie, I., and Paul, B. (2000). Can the grey mould disease of the grape-vine be controlled by yeast? FEMS Microbiology Letters 189, 233-237. 

Masih, E. I., and Paul, B. (2002). Secretion of beta -1,3-glucanases by the yeast Pichia membranaefaciens and its possible role in the biocontrol of Botrytis cinerea causing grey mould disease of the grapevine. 

Current Microbiology 44, 391-395. 

Masih, E. I., Slezack-Deschaumes, S., Marmaras, I., Barka, E. A., Vernet, G., Charpentier, C., Adholeya, A., and Paul, B. (2001). Characterisation of the yeast Pichia membranifaciens and its possible use in 

the biological control of Botrytis cinerea, causing the grey mould disease of grapevine. FEMS Microbiology Letters 202, 227-232. 

McHugh, R., and Seddon, B. (2001). Mode of action of Brevibacillus brevis - biocontrol and biorational control. Bulletin OILB/SROP 24, 17-20. 

McHugh, R., White, D., Schmitt, A., Ernst, A., and Seddon, B. (2002). Biocontrol of Botrytis cinerea infection of tomato in unheated polytunnels in the North East of Scotland. Bulletin OILB/SROP 25, 155- 

158. 

Mercier, J., and Jimenez, J. I. (2004). Control of fungal decay of apples and peaches by the biofumigant fungus Muscodor albus. Postharvest Biology and Technology 31, 1-8. 

Mercier, J., and Jimenez, J. I. (2007). Potential of the volatile-producing fungus Muscodor albus for control of building molds. Canadian Journal of Microbiology 53, 404-410. 

Meszka, B., and Bielenin, A. (2004). Possibilities of integrated grey mould control on strawberry plantations in Poland. Bulletin OILB/SROP 27, 41-45. 

Metz, C., Oerke, E. C., and Dehne, H. W. (2002). Biological control of grey mould (Botrytis cinerea) with the antagonist Ulocladium atrum. Mededelingen - Faculteit Landbouwkundige en Toegepaste 

Biologische Wetenschappen, Universiteit Gent 67, 353-359. 

Meyer, G. d., Bigirimana, J., Elad, Y., and Hofte, M. (1998). Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. European Journal of Plant Pathology 104, 279-286. 

Meyer, U. M., Fischer, E., Barbul, O., and Elad, Y. (2001). Effect of biocontrol agents on antigens present in the extracellular matrix of Botrytis cinerea, which are important for pathogenesis. Bulletin 

OILB/SROP 24, 5-9. 

Meziane, H., Chernin, L., and Hofte, M. (2006). Use of Serratia plymuthica to control fungal pathogens in bean and tomato by induced resistance and direct antagonism. Bulletin OILB/SROP 29, 101-105. 

Migheli, Q., Gullino, M. L., Piano, S., Galliano, A., and Duverney, C. (1997). Biocontrol capability of Metschnikowia pulcherrima and Pseudomonas syringae against postharvest rots of apple under semicommercial 

condition. Mededelingen - Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, Universiteit Gent 62, 1065-1070. 

Mikani, A., Etebarian, H. R., Aminian, H., and Alizadeh, A. (2007). Interaction between Pseudomonas fluorescens isolates and thiabendazole in the control of gray mold of apple. Pakistan Journal of 


Mikani, A., Etebarian, H. R., Sholberg, P. L., O'Gorman, D. T., Stokes, S., and Alizadeh, A. (2008). Biological control of apple gray mold caused by Botrytis mali with Pseudomonas fluorescens strains. 


Minuto, G., Bruzzone, C., Tinivella, F., Lodovica Gullino, M., and Garibaldi, A. (2002). Biological control in cyclamen. Colture Protette 31, 85-95. 

Minuto, G., Minuto, A., Tinivella, F., Lodovica Gullino, M., and Garibaldi, A. (2004). Disease control on organically grown cyclamen. Bulletin OILB/SROP 27, 89-93. 

Mischke, S. (1998). Mycoparasitism of selected sclerotia-forming fungi by Sporidesmium sclerotivorum. Canadian Journal of Botany 76, 460-466. 

Mizrakci, A., and Yildiz, F. (2002). Studies on the effect of calcium and a Pseudomonas fluorescens isolate to control Botrytis cinerea Pers. on tomato. Journal of Turkish Phytopathology 31, 31-41. 

Molina Mercader, G., Zaldua Flores, S., Gonzalez Vargas, G., and Sanfuentes Von Stowasser, E. (2006). Screening to antagonistic fungi for Botrytis cinerea biocontrol in Chilean forest nurseries. Bosque 27, 

126-134. 

Monchiero, M., Gilardi, G., Garibaldi, A., and Gullino, M. L. (2005). Chemical and biological control of grey mould of grapevine in North-western Italy. Informatore Fitopatologico 55, 38-44. 

94

Appendix 1 

Morandi, M. A. B., Maffia, L. A., Mizubuti, E. S. G., Alfenas, A. C., and Barbosa, J. G. (2003). Suppression of Botrytis cinerea sporulation by Clonostachys rosea on rose debris: a valuable component in 

Botrytis blight management in commercial greenhouses. Biological Control 26, 311-317. 

Morandi, M. A. B., Maffia, L. A., Mizubuti, E. S. G., Alfenas, A. C., Barbosa, J. G., and Cruz, C. D. (2006). Relationships of microclimatic variables to colonization of rose debris by Botrytis cinerea and the 

biocontrol agent Clonostachys rosea. Biocontrol Science and Technology 16, 619-630. 

Morandi, M. A. B., Maffia, L. A., and Sutton, J. C. (2001). Development of Clonostachys rosea and interactions with Botrytis cinerea in rose leaves and residues. Phytoparasitica 29, 103-113. 

Morandi, M. A. B., Maffia, L. A., and Tatagiba, J. S. (1999). Pathogenicity of Cladosporium spp. isolates, potential biocontrol agents of Botrytis cinerea, to rose plants. Summa Phytopathologica 25, 367-369. 

Morandi, M. A. B., Mattos, L. P. V., and Santos, E. R. (2007). Influence of application time on survival, establishment and ability of Clonostachys rosea to control Botrytis cinerea conidiation on rose debris. 


Morandi, M. A. B., Mattos, L. P. V., Santos, E. R., and Bonugli, R. C. (2008). Influence of application time on the establishment, survival, and ability of Clonostachys rosea to suppress Botrytis cinerea 

sporulation on rose debris. Crop Protection 27, 77-83. 

Morandi, M. A. B., Sutton, J. C., and Maffia, L. A. (2000a). Effects of host and microbial factors on development of Clonostachys rosea and control of Botrytis cinerea in rose. European Journal of Plant 

Pathology 106, 439-448. 

Morandi, M. A. B., Sutton, J. C., and Maffia, L. A. (2000b). Relationships of aphid and mite infestations to control of Botrytis cinerea by Clonostachys rosea in rose (Rosa hybrida) leaves. Phytoparasitica 28, 

55-64. 

Moreno Velandia, C. A., Cotes, A. M., and Guevara Vergara, E. (2007). Biological control of foliar diseases in tomato greenhouse crop in Colombia: selection of antagonists and efficacy tests. Bulletin 

OILB/SROP 30, 59-62. 

Moyano, C., Raposo, R., Gomez, V., and Melgarejo, P. (2003). Integrated Botrytis cinerea management in Southeastern Spanish greenhouses. Journal of Phytopathology 151, 80-85. 

Mukherjee, P. K., Haware, M. P., and Raghu, K. (1997). Induction and evaluation of benomyl-tolerant mutants of Trichoderma viride for biological control of Botrytis grey mould of chickpea. Indian 


Nadkarni, S. R., Triptikumar, M., Bhat, R. G., Gupte, S. V., and Sachse, B. (1998). Mathemycin A, a new antifungal macrolactone from actinomycete sp. HIL Y-8620959: I. fermentation, isolation, physicochemical 

properties and biological activities. Journal of Antibiotics 51, 579-581. 

Navazio, L., Baldan, B., Moscatiello, R., Zuppini, A., Woo, S. L., Mariani, P., and Lorito, M. (2007). Calcium-mediated perception and defense responses activated in plant cells by metabolite mixtures 

secreted by the biocontrol fungus Trichoderma atroviride. BMC Plant Biology 7, (30 July 2007). 

Nian, H., Zhang, J., Fan, L., Liu, S., Song, F., and Huang, D. (2007). Application of ARDRA technology in Pseudomonas fluorescens isolation and identification. Scientia Agricultura Sinica 40, 92-98. 

Nicot, P. C., Decognet, V., Bardin, M., Romiti, C., Trottin, Y., Fournier, C., and Leyre, J. M. (2003). Potential for including Microdochium dimerum, a biocontrol agent against Botrytis cinerea, into an 

integrated protection scheme of greenhouse tomatoes. In "Colloque international tomate sous abri, protection integree - agriculture biologique, Avignon, France, 17-18 et 19 septembre 2003", pp. 19-23. 

Nicot, P. C., Decognet, V., Fruit, L., Bardin, M., and Trottin, Y. (2002). Combined effect of microclimate and dose of application on the efficacy of biocontrol agents for the protection of pruning wounds on 

tomatoes against Botrytis cinerea. Bulletin OILB/SROP 25, 73-76. 

Nie, Y., Liu, Y., Li, D., Liu, Y., Luo, C., and Chen, Z. (2007). Marine bacteria with antimicrobial activity against rice sheath blight. Jiangsu Journal of Agricultural Sciences 23, 420-427. 

Nielsen, K., Yohalem, D. S., Green, H., and Jensen, D. F. (2000). Biological control of grey mould in onion. DJF Rapport, Havebrug, 55-61. 

Nobre, S. A. M., Maffia, L. A., Mizubuti, E. S. G., Cota, L. V., and Dias, A. P. S. (2005). Selection of Clonostachys rosea isolates from Brazilian ecosystems effective in controlling Botrytis cinerea. Biological 

Control 34, 132-143. 

Novikova, I. I., Litvinenko, A. I., Boikova, I. V., Yaroshenko, V. A., and Kalko, G. V. (2003). Biological activity of new microbiological preparations alirins B and S designed for plant protection against 

diseases. I. Biological activity of alirins against diseases of vegetable crops and potato. Mikologiya i Fitopatologiya 37, 92-98. 

Nunes, C., Teixido, N., Usall, J., and Vinas, I. (2001a). Biological control of major postharvest diseases on pear fruits with antagonistic bacterium Pantoea agglomerans (CPA-2). Acta Horticulturae, 403-404. 

Nunes, C., Usall, J., Teixido, N., Abadias, I., Asensio, A., and Vinas, I. (2007). Biocontrol of postharvest decay using a new strain of Pseudomonas syringae CPA-5 in different cultivars of pome fruits. 

Agricultural and Food Science 16, 56-65. 

Nunes, C., Usall, J., Teixido, N., Abadias, M., and Vinas, I. (2002a). Improved control of postharvest decay of pears by the combination of Candida sake (CPA-1) and ammonium molybdate. Phytopathology 

92, 281-287. 

Nunes, C., Usall, J., Teixido, N., Fons, E., and Vinas, I. (2002b). Postharvest biological control by Pantoea agglomerans (CPA-2) on Golden Delicious apples. Journal of Applied Microbiology 92, 247-255. 

Nunes, C., Usall, J., Teixido, N., Torres, R., and Vinas, I. (2002c). Control of Penicillium expansum and Botrytis cinerea on apples and pears with the combination of Candida sake and Pantoea agglomerans. 

Journal of Food Protection 65, 178-184. 

Nunes, C., Usall, J., Teixido, N., and Vinas, I. (2001b). Biological control of postharvest pear diseases using a bacterium, Pantoea agglomerans CPA-2. International Journal of Food Microbiology 70, 53-61. 

95


Nunes, C., Usall, J., Teixido, N., and Vinas, I. (2002d). Improvement of Candida sake biocontrol activity against post-harvest decay by the addition of ammonium molybdate. Journal of Applied Microbiology 

92, 927-935. 

Okada, A., Banno, S., Ichiishi, A., Kimura, M., Yamaguchi, I., and Fujimura, M. (2005). Pyrrolnitrin interferes with osmotic signal transduction in Neurospora crassa. Journal of Pesticide Science 30, 378-383. 

Olson, H. A., and Benson, D. M. (2007). Induced systemic resistance and the role of binucleate Rhizoctonia and Trichoderma hamatum 382 in biocontrol of Botrytis blight in geranium. Biological Control 42, 

233-241. 

Ongena, M., Giger, A., Jacques, P., Dommes, J., and Thonart, P. (2002). Study of bacterial determinants involved in the induction of systemic resistance in bean by Pseudomonas putida BTP1. European 

Journal of Plant Pathology 108, 187-196. 

Ongena, M., Jacques, P., Toure, Y., Destain, J., Jabrane, A., and Thonart, P. (2005). Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Applied 

Microbiology and Biotechnology 69, 29-38. 

Orlikowski, L. B., and Skrzyoczak, C. (2003). Biocides in the control of soil-borne and leaf pathogens. Sodininkyste ir Darzininkyste 22, 426-433. 

Orlikowski, L. B., and Skrzypczak, C. (2001). Biopreparations from grapefruit extract - progress in the biological control of plant diseases. Annales Universitatis Mariae Curie-Sklodowska. Sectio EEE, 

Horticultura 9, 261-269. 

Orlikowski, L. B., Skrzypczak, C., and Jaworska-Marosz, A. (2002). Development of Botrytis species in the presence of grapefruit extract. Bulletin OILB/SROP 25, 151-154. 

Pan, Z., Liu, W., Qiu, J., Dong, K., Tian, Z., Liu, D., and Liu, X. (2005). Effect of the actinomyces strains III-61 and A-21 on the control of Fusarium wilt and grey mould of vegetables. Acta Agriculturae 

Boreali-Sinica 20, 92-97. 

Park, H., Lee, J. Y., Hwang, I., Yun, B., Kim, B., and Hwang, B. (2006). Isolation and antifungal and antioomycete activities of staurosporine from Streptomyces roseoflavus strain LS-A24. Journal of 

Agricultural and Food Chemistry 54, 3041-3046. 

Park, J., Kirn, R., Aslam, Z., Jeon, C., and Chung, Y. (2008). Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter. 

International Journal of Systematic and Evolutionary Microbiology 58, 387-392. 

Park, S., Bae, D., Lee, J., Chung, S., and Kim, H. (1999). Integration of biological and chemical methods for the control of pepper grey mould rot under commercial greenhouse conditions. Plant Pathology 

Journal 15, 162-167. 

Paul, B. (1999a). Pythium periplocum, an aggressive mycoparasite of Botrytis cinerea causing the gray mould disease of grape-vine. FEMS Microbiology Letters 181, 277-280. 

Paul, B. (1999b). Suppression of Botrytis cinerea causing the grey mould disease of grape-vine by an aggressive mycoparasite, Pythium radiosum. FEMS Microbiology Letters 176, 25-30. 

Paul, B. (2000). Pythium contiguanum nomen novum (syn. Pythium dreschleri Paul), its antagonism to Botrytis cinerea, ITS1 region of its nuclear ribosomal DNA, and its comparison with related species. 

FEMS Microbiology Letters 183, 105-110. 

Paul, B. (2003). Characterisation of a new species of Pythium isolated from a wheat field in northern France and its antagonism towards Botrytis cinerea causing the grey mould disease of the grapevine. 

FEMS Microbiology Letters 224, 215-223. 

Paul, B. (2004). A new species of Pythium isolated from burgundian vineyards and its antagonism towards Botrytis cinerea, the causative agent of the grey mould disease. FEMS Microbiology Letters 234, 

269-274. 

Paul, B., Chereyathmanjiyil, A., Masih, I., Chapuis, L., and Benoit, A. (1998). Biological control of Botrytis cinerea causing grey mould disease of grapevine and elicitation of stilbene phytoalexin (resveratrol) 

by a soil bacterium. FEMS Microbiology Letters 165, 65-70. 

Paul, B., Girard, I., Bhatnagar, T., and Bouchet, P. (1997). Suppression of Botrytis cinerea causing grey mould disease of grape vine (Vitis vinifera) and its pectinolytic activities by a soil bacterium. 

Microbiological Research 152, 413-420. 

Pellegrini, E., Sicher, C., Fiore, A., Fogliano, V., and Pertot, I. (2007). Efficacy of Pseudomonas syringae lipodepsipeptides in inhibiting Botrytis cinerea on strawberry fruits. Bulletin OILB/SROP 30, 195-198. 

Pezet, R., Pont, V., and Tabacchi, R. (1999). Simple analysis of 6-pentyl- alpha -pyrone, a major antifungal metabolite of Trichoderma spp., useful for testing the antagonistic activity of these fungi. 

Phytochemical Analysis 10, 285-288. 

Piano, S., Cerchio, F., Migheli, Q., and Gullino, M. L. (1998). Effect of different substances on biocontrol activity of the antagonistic yeast Metschnikowia pulcherrima 4.4 against Botrytis cinerea and on his 

survival on apple. Atti, Giornate fitopatologiche, Scicli e Ragusa, 3-7 maggio, 1998, 495-500. 

Pradeep, K., Anuja, and Kumud, K. (2000). Bio-control of seed-borne fungal pathogens of pigeonpea (Cajanus cajan (L.) Millsp.). Annals of Plant Protection Sciences 8, 30-32. 

Pristchepa, L., Voitka, D., Kasperovich, E., and Stepanova, N. (2006). Influence of Trichodermin-BL on the decrease of fiber flax infection by diseases and the improvement of ITS production quality. Journal 

of Plant Protection Research 46, 97-102. 

Prokkola, S., and Kivijarvi, P. (2007). Effect of biological sprays on the incidence of grey mould, fruit yield and fruit quality in organic strawberry production. Agricultural and Food Science 16, 25-33. 

Prokkola, S., Kivijarvi, P., and Parikka, P. (2003). Effects of biological sprays, mulching materials, and irrigation methods on grey mould in organic strawberry production. Acta Horticulturae, 169-175. 

Qian, Y., Yang, C., Ji, Z., Li, J., Long, J., and Wu, W. (2006). Antifungal metabolites of endophytic fungus A10 in Celastrus angulatus. Chinese Journal of Biological Control 22, 150-154. 

96

Appendix 1 

Rabea, E. I., Badawy, M. E. I., Rogge, T. M., Stevens, C. V., Smagghe, G., Hofte, M., and Steurbaut, W. (2003). Synthesis and biological activity of new chitosan derivatives against pest insects and fungi. 

Communications in Agricultural and Applied Biological Sciences 68, 135-138. 

Rabosto, X., Carrau, M., Paz, A., Boido, E., Dellacassa, E., and Carrau, F. M. (2006). Grapes and vineyard soils as sources of microorganisms for biological control of Botrytis cinerea. American Journal of 

Enology and Viticulture 57, 332-338. 

Ramin, A. A., Prange, R. K., Braun, P. G., and Delong, J. M. (2008). Biocontrol of postharvest fungal apple decay at 20 deg C with Muscodor albus volatiles. Acta Horticulturae, 329-335. 

Ran, L., Xiang, M., Zhou, B., and Bakker, P. A. H. M. (2005). Siderophores are the main determinants of fluorescent Pseudomonas strains in suppression of grey mould in Eucalyptus urophylla. Acta 

Phytopathologica Sinica 35, 6-12. 

Raoof, M. A., Mehtab, Y., and Rana, K. (2003). Potential of biocontrol agents for the management of castor grey mold, Botrytis ricini Godfrey. Indian Journal of Plant Protection 31, 124-126. 

Razak, A. A., Soliman, H. G., El-Sheikh, H. H., and Farrag, A. A. (2000). Physiological consequences of Botrytis fabae on Vicia faba plant. African Journal of Mycology and Biotechnology 8, 39-50. 

Reglinski, T., Elmer, P. A. G., Taylor, J. T., Parry, F. J., Marsden, R., and Wood, P. N. (2005). Suppression of Botrytis bunch rot in Chardonnay grapevines by induction of host resistance and fungal 

antagonism. Australasian Plant Pathology 34, 481-488. 

Rey, M., Delgado-Jarana, J., and Benitez, T. (2001). Improved antifungal activity of a mutant of Trichoderma harzianum CECT 2413 which produces more extracellular proteins. Applied Microbiology and 

Biotechnology 55, 604-608. 

Ricard, T., and Jorgensen, H. (2000). BINAB's effective, economical, and environment compatible Trichoderma products as possible Systemic Acquired Resistance (SAR) inducers in strawberries. DJF 

Rapport, Havebrug, 67-75. 

Roudet, J., and Dubos, B. (2001). Efficacy and mode of action of Ulocladium atrum against grey mold on grapevine. Bulletin OILB/SROP 24, 73-77. 

Saad, M. M., Saad, A. M., and Hassan, H. M. (2005). Biological control of the pathogenic fungus Botrytis cinerea on bean leaves by using Bacillus subtilis and Bacillus megaterium. African Journal of 

Mycology and Biotechnology 13, 21-34. 

Sadfi-Zouaoui, N., Essghaier, B., Hajlaoui, M. R., Achbani, H., and Boudabous, A. (2007a). Ability of the antagonistic bacteria Bacillus subtilis and B. licheniformis to control Botrytis cinerea on fresh-market 

tomatoes. Bulletin OILB/SROP 30, 63. 

Sadfi-Zouaoui, N., Essghaier, B., Hajlaoui, M. R., Fardeau, M. L., Cayaol, J. L., Ollivier, B., and Boudabous, A. (2008). Ability of moderately halophilic bacteria to control grey mould disease on tomato 

fruits. Journal of Phytopathology 156, 42-52. 

Sadfi-Zouaoui, N., Essghaier, B., Hannachi, I., Hajlaoui, M. R., and Boudabous, A. (2007b). First report on the use of moderately halophilic bacteria against stem canker of greenhouse tomatoes caused by 

Botrytis cinerea. Annals of Microbiology 57, 337-339. 

Salas Brenes, W., and Sanchez Garita, V. (2006). Biological control of Botrytis cinerea on pepper and tomato crops under greenhouse conditions. Manejo Integrado de Plagas y Agroecologia, 56-62. 

Saligkarias, I. D., Gravanis, F. T., and Epton, H. A. S. (2002). Biological control of Botrytis cinerea on tomato plants by the use of epiphytic yeasts Candida guilliermondii strains 101 and US 7 and Candida 

oleophila strain I-182: II. A study on mode of action. Biological Control 25, 151-161. 

Sansone, G., Rezza, I., Calvente, V., Benuzzi, D., and Sanz de Tosetti, M. I. (2005). Control of Botrytis cinerea strains resistant to iprodione in apple with rhodotorulic acid and yeasts. Postharvest Biology and 


Santorum, P., Garcia-Roig, M., Azpilicueta, A., Llobell, A., and Monte, E. (2002). Trichoderma protein ability in preventing grey mould and anthracnose diseases on strawberry leaves and petioles. Bulletin 

OILB/SROP 25, 257-260. 

Santos, A., and Marquina, D. (2004). Killer toxin of Pichia membranifaciens and its possible use as a biocontrol agent against grey mould disease of grapevine. Microbiology (Reading) 150, 2527-2534. 

Santos, A., Sanchez, A., and Marquina, D. (2004). Yeasts as biological agents to control Botrytis cinerea. Microbiological Research 159, 331-338. 

Sanz, L., Montero, M., Grondona, I., Llobell, A., and Monte, E. (2002). In vitro antifungal activity of Trichoderma harzianum, T. longibrachiatum, T. asperellum and T. atroviride against Botrytis cinerea 

pathogenic to strawberry. Bulletin OILB/SROP 25, 253-256. 

Sanz, L., Montero, M., Redondo, J., Llobell, A., and Monte, E. (2005). Expression of an alpha -1,3- glucanase during mycoparasitic interaction of Trichoderma asperellum. FEBS Journal 272, 493-499. 

Sardi, P., Saracchi, M., and Farina, G. (2008). Antifungal activity of Bacillus subtilis against rot pathogens. In "Giornate Fitopatologiche 2008, Cervia", pp. 565-572. 

Schena, L., Ippolito, A., Zahavi, T., Cohen, L., Nigro, F., and Droby, S. (1999). Genetic diversity and biocontrol activity of Aureobasidium pullulans isolates against postharvest rots. Postharvest Biology and 


Schilder, A. M. C., Gillett, J. M., Sysak, R. W., and Wise, J. C. (2002). Evaluation of environmentally friendly products for control of fungal diseases of grapes. In "10th International Conference on 

Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing and Viticulture. Proceedings of a conference, Weinsberg, Germany, 4-7 February 2002", pp. 163-167. 

Schmitt, A., Malathrakis, N., Konstantinidou-Doltsinis, S., Dik, A., Ernst, A., Francke, W., Petsikos-Panayotarou, N., Schuld, M., and Seddon, B. (2001). Improved plant health by the combination of 

biological disease control methods. Bulletin OILB/SROP 24, 29-32. 

Schoene, P., and Köhl, J. (1999). Biological control of Botrytis cinerea by Ulocladium atrum in grapevine and Cyclamen. Gesunde Pflanzen 51, 81-85. 

97


Schoene, P., Lennartz, B., and Oerke, E. C. (1999). Fungicide sensitivity of fungi used for biocontrol of perthotrophic pathogens. In "Modern fungicides and antifungal compounds II. 12th International 

Reinhardsbrunn Symposium, Friedrichroda, Thuringia, Germany, 24th-29th May 1998." pp. 477-482. 

Schoene, P., Oerke, E. C., and Dehne, H. W. (2000). A new concept for integrated control of grey mould (Botrytis cinerea) in grapevine. In "The BCPC Conference: Pests and diseases, Volume 3. Proceedings 

of an international conference held at the Brighton Hilton Metropole Hotel, Brighton, UK, 13-16 November 2000", pp. 1031-1036. 

Schoonbeek, H. J., Jacquat-Bovet, A. C., Mascher, F., and Metraux, J. P. (2007). Oxalate-degrading bacteria can protect Arabidopsis thaliana and crop plants against Botrytis cinerea. Molecular Plant-Microbe 

Interactions 20, 1535-1544. 

Schotsmans, W. C., Braun, G., DeLong, J. M., and Prange, R. K. (2008). Temperature and controlled atmosphere effects on efficacy of Muscodor albus as a biofumigant. Biological Control 44, 101-110. 

Seddon, B., McHugh, R. C., and Schmitt, A. (2000). Brevibacillus brevis - a novel candidate biocontrol agent with broad-spectrum antifungal activity. In "The BCPC Conference: Pests and diseases, Volume 

2. Proceedings of an international conference held at the Brighton Hilton Metropole Hotel, Brighton, UK, 13-16 November 2000", pp. 563-570. 

Seddon, B., and Schmitt, A. (1999). Integrated biological control of fungal plant pathogens using natural products. In "Modern fungicides and antifungal compounds II. 12th International Reinhardsbrunn 

Symposium, Friedrichroda, Thuringia, Germany, 24th-29th May 1998." pp. 423-428. 

Sesan, T. E., Stefan, A. L., Constantinescu, F., and Petrescu, A. (2002). Grapevine rots - diseases coming back into actuality in viticulture. II. Biological control. Analele Institutului de Cercetare-Dezvoltare 

pentru Protectia Plantelor 32, 167-174. 

Shafir, S., Dag, A., Bilu, A., Abu-Toamy, M., and Elad, Y. (2006). Honey bee dispersal of the biocontrol agent Trichoderma harzianum T39: effectiveness in suppressing Botrytis cinerea on strawberry under 

field conditions. European Journal of Plant Pathology 116, 119-128. 

Sharga, B. M. (1997). Bacillus isolates as potential biocontrol agents against chocolate spot on faba beans. Canadian Journal of Microbiology 43, 915-924. 

Shentu, X., Chen, X., and Yu, X. (2006). The isolation of endophytic fungi from Tripterygiun wilfordii Hook and the screening of its active strain. Acta Agriculturae Zhejiangensis 18, 308-312. 

Shipp, L., Kapongo, J. P., Kevan, P., Sutton, J., and Broadbent, B. (2008). Using bees to disseminate multiple fungal agents for insect pest control and plant disease suppression in greenhouse vegetables. 


Silva-Ribeiro, R. T., Termignoni, C., Dillon, A. J. P., and Henriques, J. A. P. (2001). Lethal effect of five Trichoderma spp. strains on the plant pathogen Botrytis cinerea. Summa Phytopathologica 27, 364- 

369. 

Smolinska, U., and Kowalska, B. (2006). The effectivity of plant extracts and antagonistic microorganisms on the growth inhibition of French bean pathogenic fungi. Vegetable Crops Research Bulletin 64, 

67-76. 

Sobiczewski, P., and Bryk, H. (1999). The possibilities and limitations of biological control of apples against gray mold and blue mold with bacteria Pantoea agglomerans and Pseudomonas sp. Progress in 

Plant Protection 39, 139-147. 

Solis, C., Becerra, J., Flores, C., Robledo, J., and Silva, M. (2004). Antibacterial and antifungal terpenes from Pilgerodendron uviferum (D. Don) Florin. Journal of the Chilean Chemical Society 49, 157-161. 

Someya, N., Nakajima, M., Hirayae, K., Hibi, T., and Akutsu, K. (2001). Synergistic antifungal activity of chitinolytic enzymes and prodigiosin produced by biocontrol bacterium, Serratia marcescens strain 

B2 against gray mold pathogen, Botrytis cinerea. Journal of General Plant Pathology 67, 312-317. 

Son, Y., Lee, J., Kim, C., Song, J., Kim, H., Kim, J., Kim, D., Park, H., and Moon, B. (2002). Biological control of gray mold rot of perilla caused by Botrytis cinerea. I. Resistance of perilla cultivars and 

selection of antagonistic bacteria. Plant Pathology Journal 18, 36-42. 

Spadaro, D., Garibaldi, A., and Gullino, M. L. (2004). Control of Penicillium expansum and Botrytis cinerea on apple combining a biocontrol agent with hot water dipping and acibenzolar-S-methyl, baking 

soda, or ethanol application. Postharvest Biology and Technology 33, 141-151. 

Spadaro, D., Vola, R., Piano, S., and Gullino, M. L. (2002). Mechanisms of action and efficacy of four isolates of the yeast Metschnikowia pulcherrima active against postharvest pathogens on apples. 


Stensvand, A. (1997). Evaluation of two new fungicides and a biocontrol agent against grey mould in strawberries. Tests of Agrochemicals and Cultivars, 22-23. 

Stensvand, A. (1998). Evaluation of new fungicides and a biocontrol agent against grey mould in strawberries. Tests of Agrochemicals and Cultivars, 70-71. 

Stevenson, P. C., and Haware, M. P. (1999). Maackiain in Cicer bijugum Rech. f. associated with resistance to Botrytis grey mould. Biochemical Systematics and Ecology 27, 761-767. 

Stompor-Chrzan, E. (2002). Effect of aqueous extracts of aspen, black currant, folded blackberry and walnut leaves on development of pathogenic fungi. Plant Protection Science 38, 623-625. 

Stowasser, E. S. v., and Ferreira, F. A. (1997). Evaluation of fungi for biological control of Botrytis cinerea in eucalyptus nurseries. Revista Arvore 21, 147-153. 

Stromeng, G. M., Hjeljord, L. G., Dobson, A., Stensvand, A., and Tronsmo, A. (2006). Control of grey mould (Botrytis cinerea) in strawberry using fungal antagonists. Bulletin OILB/SROP 29, 9-13. 

Sugar, D., and Benbow, J. M. (2002). Effect of short-term exposure to high CO2 in combination with biological control on postharvest decay of pears, and factors affecting sensitivity of pears to CO2 injury. 

Acta Horticulturae, 891-894. 

Sun, Y., Zeng, H., Shi, Y., and Li, G. (2003). Mode of action of wuyiencin on Botrytis cinerea. Acta Phytopathologica Sinica 33, 434-438. 

Sun, Y., Zong, H., Shi, Y., Li, G., and Wang, X. (2004). Inhibition of Botrytis cinerea by wuyiencin and variation of enzyme activities associated with disease resistance in tomato. Plant Protection 30, 45-48. 

98

Appendix 1 

Sutton, J. C., Liu, W., Huang, R., and Owen-Going, N. (2002). Ability of Clonostachys rosea to establish and suppress sporulation potential of Botrytis cinerea in deleafed stems of hydroponic greenhouse 

tomatoes. Biocontrol Science and Technology 12, 413-425. 

Swadling, I. R., and Jeffries, P. (1998). Antagonistic properties of two bacterial biocontrol agents of grey mould disease. Biocontrol Science and Technology 8, 439-448. 

Szandala, E. S., and Backhouse, D. (2001). Suppression of sporulation of Botrytis cinerea by antagonists applied after infection. Australasian Plant Pathology 30, 165-170. 

Tatagiba, J. S. d., Maffia, L. A., Barreto, R. W., Alfenas, A. C., and Sutton, J. C. (1998). Biological control of Botrytis cinerea in residues and flowers of rose (Rosa hybrida). Phytoparasitica 26, 8-19. 

Tehrani, A. S., and Alizadeh, H. (2000). Biocontrol of Botrytis cinerea the causal agent of gray mold of strawberry by antagonistic fungi. Mededelingen - Faculteit Landbouwkundige en Toegepaste 

Biologische Wetenschappen, Universiteit Gent 65, 617-629. 

Teichmann, B., Linne, U., Hewald, S., Marahiel, M. A., and Bolker, M. (2007). A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Molecular 


Tian, S., Fan, Q., Xu, Y., and Liu, H. (2002). Biocontrol efficacy of antagonist yeasts to gray mold and blue mold on apples and pears in controlled atmospheres. Plant Disease 86, 848-853. 

Tian, S., Qin, G., and Xu, Y. (2004a). Survival of antagonistic yeasts under field conditions and their biocontrol ability against postharvest diseases of sweet cherry. Postharvest Biology and Technology 33, 

327-331. 

Tian, X., Long, J., Bai, H., and Wu, W. (2004b). Studies on the fungicidal activity of secondary metabolic products of Actinomycetales. Plant Protection 30, 51-54. 

Tirupathi, J., Kumar, C. P. C., and Reddy, D. R. R. (2006). Trichoderma as potential biocontrol agents for the management of grey mold of castor. Journal of Research ANGRAU 34, 31-36. 

Toure, Y., Ongena, M., Jacques, P., Guiro, A., and Thonart, P. (2004). Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. 

Journal of Applied Microbiology 96, 1151-1160. 

Trotel-Aziz, P., Aziz, A., Amborabe, E., Kilani-Feki, O., and Vernet, G. (2003). Biological control of Botrytis cinerea in vineyards (Vitis vinifera L.): evaluation of native endophytic bacteria of the 

Champagne Ardenne region. Progres Agricole et Viticole 120, 279-280. 

Trottin-Caudal, Y., Fournier, C., Leyre, J. M., Nicot, P., Decognet, V., Bardin, M., and Romiti, C. (2001). Protected tomato: biological control of Botrytis cinerea and Oidium neolycopersici. PHM Revue 

Horticole, xiii-xv. 

Tsomlexoglou, E., Allan, E. J., and Seddon, B. (2000). Biocontrol strategies for Bacillus antagonists to tomato grey mould Botrytis cinerea) based on the mode of action and disease suppression. In "The 

BCPC Conference: Pests and diseases, Volume 3. Proceedings of an international conference held at the Brighton Hilton Metropole Hotel, Brighton, UK, 13-16 November 2000", pp. 1037-1042. 

Tsomlexoglou, E., Seddon, B., and Allan, E. J. (2001). Biocontrol potential of Bacillus antagonists selected for their different modes of action against Botrytis cinerea. Bulletin OILB/SROP 24, 137-141. 

Tsomlexoglou, E., Seddon, B., and Allan, E. J. (2002). Influence of environmental factors on the performance of two biocontrol agents against the grey mould pathogen (Botrytis cinerea) in glasshouse-grown 

tomato crops. Bulletin OILB/SROP 25, 215-218. 

Turcanu, P. (1997). Preliminary results on the biological control of the fungus Sclerotinia fuckeliana (De Bary) F.C. at the Iasi Viticultural Research Station. Cercetari Agronomice in Moldova 30, 153-157. 

Tylkowska, K., and Szopinska, D. (1998). Effects of fungicides and Penicillium spp. and Trichoderma spp. on health and germination of onion seed. Roczniki Akademii Rolniczej w Poznaniu, Ogrodnictwo, 

339-344. 

Utkhede, R., and Bogdanoff, C. (2003). Influence of lysozyme, yeast, azoxystrobin, and myclobutanil on fungal diseases of cucumbers grown hydroponically. Crop Protection 22, 315-320. 

Utkhede, R., Bogdanoff, C., and McNevin, J. (2001). Effects of biological and chemical treatments on Botrytis stem canker and fruit yield of tomato under greenhouse conditions. Canadian Journal of Plant 

Pathology 23, 253-259. 

Utkhede, R. S., and Mathur, S. (2002). Biological control of stem canker of greenhouse tomatoes caused by Botrytis cinerea. Canadian Journal of Microbiology 48, 550-554. 

Utkhede, R. S., and Mathur, S. (2006). Preventive and curative biological treatments for control of Botrytis cinerea stem canker of greenhouse tomatoes. BioControl 51, 363-373. 

Vicedo, B., Leyva, M. d. l. O., Flors, V., Finiti, I., Amo, G. d., Walters, D., Real, M. D., Garcia-Agustin, P., and Gonzalez-Bosch, C. (2005). Control of the phytopathogen Botrytis cinerea using adipic acid 

monoethyl ester. Archives of Microbiology 184, 316-326. 

Vinas, I., Usall, J., Teixido, N., and Sanchis, V. (1998). Biological control of major postharvest pathogens on apple with Candida sake. International Journal of Food Microbiology 40, 9-16. 

Wagner, A., Kordowska-Wiater, M., and Hetman, B. (2006). Effect of some yeast strains on grey mould development on apple fruit. Progress in Plant Protection 46, 625-628. 

Walker, R., Ferguson, C. M. J., Booth, N. A., and Allan, E. J. (2002). The symbiosis of Bacillus subtilis L-forms with Chinese cabbage seedlings inhibits conidial germination of Botrytis cinerea. Letters in 


Walker, R., Innes, C. M. J., and Allan, E. J. (2001). The potential biocontrol agent Pseudomonas antimicrobica inhibits germination of conidia and outgrowth of Botrytis cinerea. Letters in Applied 


Walter, M., Zydenbos, S. M., Jaspers, M. V., and Stewart, A. (2006). Laboratory assays for selection of Botrytis suppressive micro-organisms on necrotic grape leaf discs. New Zealand Plant Protection 59, 

348-354. 

99


Wang, A., Lou, B., and Xu, T. (2007a). Inhibitory effect of the secretion of Pythium oligandrum on plant pathogenic fungi and the control effect against tomato gray mould. Acta Phytophylacica Sinica 34, 57- 

60. 

Wang, C., Sun, Z., Liu, Y., Zheng, D., Liu, X., and Li, S. (2007b). Earthworm polysaccharide and its antibacterial function on plant-pathogen microbes in vitro. European Journal of Soil Biology 43, S135- 

S142. 

Wang, G., Lu, S., Zheng, B., and Zhang, C. (2008a). Studies on metabolites of Trichoderma taxi ZJUF0986 and its inhibitory effect to tomato grey mold disease. Acta Agriculturae Zhejiangensis 20, 104-108. 

Wang, M., Chen, J., Xue, L., and He, Y. (2008b). Identification and culturing conditions of endophytic antagonistic strains associated with tomato. Zhongguo Shengtai Nongye Xuebao / Chinese Journal of 

Eco-Agriculture 16, 441-445. 

Wang, Y., Hu, W., and Xu, L. (2008c). Identification of the antagonistic Bacillus strains on melon fruit surface. Acta Phytopathologica Sinica 38, 317-324. 

Weeds, P. L., Beever, R. E., and Long, P. G. (2000). Competition between aggressive and non-aggressive strains of Botrytis cinerea (Botryotinia fuckeliana) on French bean leaves. Australasian Plant 

Pathology 29, 200-204. 

White, D., Ernst, A., Schmitt, A., and Seddon, B. (2001). Interaction of the biocontrol agent Brevibacillus brevis with other disease control methods. Bulletin OILB/SROP 24, 229-232. 

White, G. J., and Traquair, J. A. (2006). Necrotrophic mycoparasitism of Botrytis cinerea by cellulolytic and ligninocellulolytic basidiomycetes. Canadian Journal of Microbiology 52, 508-518. 

Wisniewski, M., Wilson, C., El-Ghaouth, A., and Droby, S. (2001). Increasing the ability of the biocontrol product, Aspire, to control postharvest diseases of apple and peach with the use of additives. Bulletin 

OILB/SROP 24, 157-160. 

Witkowska, D., and Maj, A. (2002). Production of lytic enzymes by Trichoderma spp. and their effect on the growth of phytopathogenic fungi. Folia Microbiologica 47, 279-282. 

Woo, S., Fogliano, V., Scala, F., and Lorito, M. (2002). Synergism between fungal enzymes and bacterial antibiotics may enhance biocontrol. Antonie van Leeuwenhoek 81, 353-356. 

Wszelaki, A. L., and Mitcham, E. J. (2003). Effect of combinations of hot water dips, biological control and controlled atmospheres for control of gray mold on harvested strawberries. Postharvest Biology and 


Xi, L., and Tian, S. (2005). Control of postharvest diseases of tomato fruit by combining antagonistic yeast with sodium bicarbonate. Scientia Agricultura Sinica 38, 950-955. 

Xiao, L., Yang, X., Dai, L., Qiu, D., Liu, Z., and Yuan, J. (2005). Antibiotic activities and properties of metabolites from Xenorhabdus sp. CB43. Journal of Hunan Agricultural University 31, 412-414. 

Yan, S., Yang, Q., and Chen, Y. (2004). Antagonism of complex microbial fertilizer and functional actinomycetes against soil-borne plant pathogenic fungi. Chinese Journal of Biological Control 20, 49-52. 

Yang, X., Liu, W., Lu, C., Qiu, J., and Wang, H. (2007). Biocontrol effect and the taxonomy of antagonistic actinomyces strain A03. Acta Phytophylacica Sinica 34, 73-77. 

Yao, M., Tu, X., Huang, L., Wang, M., Alimas, and Kang, Z. (2007). Screening of antagonistic endophytic actinomycetes against tomato. Pathogens and biological control effect on tomato leaf mould. 

Journal of Northwest A & F University - Natural Science Edition 35, 146-150. 

Yildiz, F., Yildiz, M., Delen, N., Coskuntuna, A., Kinay, P., and Turkusay, H. (2007). The effects of biological and chemical treatment on gray mold disease in tomatoes grown under greenhouse conditions. 

Turkish Journal of Agriculture and Forestry 31, 319-325. 

Yohalem, D. (1997). Prospects for the biological control of foliar plant diseases in Danish greenhouses. SP Rapport - Statens Planteavlsforsog, 199-206. 

Yohalem, D., Brodsgaard, H. F., and Enkegaard, A. (1998). Interaction of Verticillium lecanii (Mycotal) and Trichoderma harzianum (Trichodex) for control of white flies and grey mould on tomatoes: a 

preliminary report. DJF Rapport, Markbrug, 217-222. 

Yohalem, D. S. (2000). Microbial management of early establishment of grey mould in pot roses. DJF Rapport, Havebrug, 97-102. 

Yohalem, D. S. (2001). Microbiological management of foliar pathogens in glasshouses. DJF Rapport, Markbrug, 65-70. 

Yohalem, D. S. (2004). Evaluation of fungal antagonists for grey mould management in early growth of pot roses. Annals of Applied Biology 144, 9-15. 

Yohalem, D. S., and Kristensen, K. (2004). Optimization of timing and frequency of application of the antagonist Ulocladium atrum for management of gray mold in potted rose under high disease pressure. 


Yohalem, D. S., Nielsen, K., Green, H., and Jensen, D. F. (2004). Biocontrol agents efficiently inhibit sporulation of Botrytis aclada on necrotic leaf tips but spread to adjacent living tissue is not prevented. 

FEMS Microbiology Ecology 47, 297-303. 

Yohalem, D. S., Paaske, K., Kristensen, K., and Larsen, J. (2007). Single application prophylaxis against gray mold in pot rose and pelargonium with Ulocladium atrum. Biological Control 41, 94-98. 

Yu, T., Chen, J., Chen, R., Huang, B., Liu, D., and Zheng, X. (2007). Biocontrol of blue and gray mold diseases of pear fruit by integration of antagonistic yeast with salicylic acid. International Journal of 

Food Microbiology 116, 339-345. 

Yu, T., Zhang, H., Li, X., and Zheng, X. (2008). Biocontrol of Botrytis cinerea in apple fruit by Cryptococcus laurentii and indole-3-acetic acid. Biological Control 46, 171-177. 

Yu, T., and Zheng, X. (2007). An integrated strategy to control postharvest blue and grey mould rots of apple fruit by combining biocontrol yeast with gibberellic acid. International Journal of Food Science & 


Zaccardelli, M., Galdo, A. d., Campanile, F., and Giordano, I. (2006). Biological and genetic diversity of thermal-resistant bacteria isolated from different organs of garden solanaceous. Italus Hortus 13, 805- 

808. 

100

Appendix 1 

Zahavi, T., Cohen, L., Weiss, B., Schena, L., Daus, A., Kaplunov, T., Zutkhi, J., Ben-Arie, R., and Droby, S. (2000). Biological control of Botrytis, Aspergillus and Rhizopus rots on table and wine grapes in 

Israel. Postharvest Biology and Technology 20, 115-124. 

Zakharchenko, N. S., Georgievskaya, E. B., Shkolnaya, L. A., Yukhmanova, A. A., Kashparov, I. A., Buryanov, Y. I., Maslienko, L. V., Shipievskaya, E. Y., and Shevelukha, V. S. (2007). Isolation and 

characteristics of a Bacillus subtilis K-1-1 polypeptide, an inhibitor of phytopathogenous fungi and bacteria growth. Biotekhnologiya, 21-26. 

Zanella, A., Degasperi, S., Lindner, L., Marschall, K., and Pernter, P. (2003). Biocontrol of fungal rot on diphenylamine treated apple fruit by means of the natural antagonist Candida sake (CPA-1). Acta 


Zhang, C., Zheng, B., Lao, J., Mao, L., Chen, S., Kubicek, C. P., and Lin, F. (2008). Clavatol and patulin formation as the antagonistic principle of Aspergillus clavatonanicus, an endophytic fungus of Taxus 

mairei. Applied Microbiology and Biotechnology 78, 833-840. 

Zhang, H., Wang, L., Dong, Y., Jiang, S., Cao, J., and Meng, R. (2007a). Postharvest biological control of gray mold decay of strawberry with Rhodotorula glutinis. Biological Control 40, 287-292. 

Zhang, H., Zheng, X., Fu, C., and Xi, Y. (2005). Postharvest biological control of gray mold rot of pear with Cryptococcus laurentii. Postharvest Biology and Technology 35, 79-86. 

Zhang, H., Zheng, X., and Yu, T. (2007b). Biological control of postharvest diseases of peach with Cryptococcus laurentii. Food Control 18, 287-291. 

Zhang, P. G., Hopkin, A. A., and Sutton, J. C. (1996). Fungus shown to be an effective biological control of gray mold on container-grown conifers. In "Frontline, Technical Note - Great Lakes Forestry 

Centre, Canadian Forest Service", pp. 3 pp. 

Zhao, J., Li, J., and Kong, F. (2003). Biocontrol activity against Botrytis cinerea by Bacillus subtilis 728 isolated from marine environment. Annals of Microbiology 53, 29-35. 

Zhao, L., Song, J., Yang, H., Gao, Q., and Wang, J. (1998). Preliminary studies on a strain of Streptomyces used in biocontrol. Chinese Journal of Biological Control 14, 18-20. 

Zhao, Y., Shao, X., Tu, K., and Chen, J. (2007). Inhibitory effect of Bacillus subtilis B10 on the diseases of postharvest strawberry. Journal of Fruit Science 24, 339-343. 

Zhao, Y., Tu, K., Shao, X. F., Jing, W., Yang, J. L., and Su, Z. P. (2008). Biological control of the post-harvest pathogens Alternaria solani, Rhizopus stolonifer, and Botrytis cinerea on tomato fruit by Pichia 

guilliermondii. Journal of Horticultural Science and Biotechnology 83, 132-136. 

Zheng, X., Zhang, H., and Xi, Y. (2003). Postharvest biological control of gray mold rot of strawberry with Cryptococcus laurentii. Transactions of the Chinese Society of Agricultural Engineering 19, 171- 

175. 

Zheng, Y., Yao, J., Shao, X., and Muralee, N. (2000). Preliminary study on the biological activity of Sophora flavescens. Plant Protection 26, 17-19. 

Zheng, Y., Yao, J., Shao, X., and Nair, M. (1999). Preliminary study on the biological activity of Sophora flavescens Ait. Plant Protection 25, 17-19. 

Zhou, T., Chu, C., Liu, W. T., and Schaneider, K. E. (2001). Postharvest control of blue mold and gray mold on apples using isolates of Pseudomonas syringae. Canadian Journal of Plant Pathology 23, 246- 

252. 

Zhou, T., Northover, J., Schneider, K. E., and Lu, X. (2002). Interactions between Pseudomonas syringae MA-4 and cyprodinil in the control of blue mold and gray mold of apples. Canadian Journal of Plant 

Pathology 24, 154-161. 

Zoffoli, J. P., Latorre, B. A., Daire, N., and Viertel, S. (2005). Effectiveness of chlorine dioxide as influenced by concentration, pH, and exposure time on spore germination of Botrytis cinerea, Penicillium 

expansum and Rhizopus stolonifer. Ciencia e Investigacion Agraria 32, 181-188. 

101


successful effect against powdery mildew in laboratory experiments and field trials on selected crops. 

Powdery mildew on cereals 



Bacteria 

Pseudomonas aureofaciens ; Bacillus subtilis ; P. fluorescens 

(Sanin et al., 2008) 

General paper: 

Crop protection: management strategies (Prasad, 2005) 

M 


Bacteria 

Rhizobacteria (Yigit, 2004) 

Bacteria, (Azarang, 2004) 


Acremonium alternatum (Kasselaki, 2006a, b) 

Alternaria alternata, Aspergillus niger, Bipolaris spicifera, Cladosporium cladosporioides, Curvularia lunata, 

Fusarium acuminatum F. semitectum, Penicillium rubrum, (Simian, 2008) 

BCAs mix (David, 2007) 

Fungi (Azarang, 2004) 

Fusarium oxysporum f. sp. radicis-lycopersici (Nelson, 2005) 

Paecilomyces farinosus (Szentivanyi, 2006) 

Verticillium lecanii (Koike, 2004) 

B Bryophyte extracts (Tadesse, 2003) 

Aromatic substances (Koitabashi, 2002) 

Mycelial extracts (Haugaard, 2002) 

O 

PAF from Penicillium chrysogenum (Barna, 2008) 

Secondary metabolic products of strain A19 of actinomycetes (Shen et al., 2008) 

Verlamelin (Kim, 2002) 

Powdery mildew on pome/stone fruits 


Bacteria 


yeast (Y16) (Alaphilippe, 2007) 

M 

B 

O 



Bacteria 


Ampelomyces quisqualis (Harvey, 2006) 

Ampelomyces quisqualis (Sonali, 2005) 

yeast (Y16) (Alaphilippe, 2008) 

102

Appendix 2 

Powdery mildew on grapes 


Bacteria 

Bacillus subtilis (Crisp, 2006) 

Photosynthetic bacteria (Robotic, 2002) 


Ampelomyces hyperparasites (Fuzi, 2003) 

Ampelomyces quisqualis (Angeli, 2006a, b, c, 2007a, b) 

Ampelomyces quisqualis (Hoffmann, 2007) 

Ampelomyces quisqualis 94013 (Lee, 2004) 

M 

BCAs (Amaro, 2003) 

BCAs (Ari, 2004) 

BCAs (Kaine, 2003) 

BCAs (Linder et al., 2006) 

BCAs (Zulini, 2004) 

Pseudozyma flocculosa (Schmitt, 2001) 

Yeast (Robotic, 2002) 

B 

O 

Milsana (VP99) (Schmitt, 2001, 2002) 

fresh or dried milk (10%),pinolene 1%, calcium chloride (2%), 

tripotassium phosphate (1%) and a mixture of mineral oil 

(1%),sodium bicarbonate/sodium silicate (0.5%) (Casulli, 2002) 

mycophagous mite (Melidossian, 2005) 



Bacteria 

Brevibacillus brevis (Schmitt, 2001, 2002) 

PGPR (Konstantinidou-Doltsinis, 2007) 

Pseudomonas syringes pv. Syringe (Kassemeyer, 1998) 

Serenade (Bacillus subtilis)(Schilder, 2002) 


Ampelomyces quisqualis (Angeli, 2006a, b, c, 2007a, b) 

Ampelomyces quisqualis 94013 (Lee, 2004) 

Ampelomyces quisqualis AQ10, (Schweigkofler, 2006) 

BCA mix (David, 2007) 

BCAs (Kaine, 2003) 

BCAs {Amaro, 2003 #177 

Pseudozyma flocculosa (Schmitt, 2001) 

Pseudozyma flocculosa (SporodexReg. L) (Konstantinidou-Doltsinis, 2007) 

Tilletiopsis spp (Haggag, 2007) 

Milsana (VP99) (Konstantinidou-Doltsinis, 2001) 

Milk, whey, whey protein, Bacillus subtilis, yeast extract medium (Crisp, 2006) 

Mycophagous mite (Melidossian, 2005) 

Orthotydeus lambi mites (English-Loeb, 1999, 2006, 2007) 

Powdery mildew on strawberry pathogen: Podosphaera aphanis f.sp. fragariae; Sphaerotheca macularis f.sp. fragariae 



Bacteria 


Bacteria 

B. subtilis QST (Fiamingo, 2007a) 

Bacillus subtilis (Amsalem, 2004) 

Bacillus subtilis (Pertot, 2004) (Pertot, 2008) 

Pseudomonas reactans (Fiamingo, 2007b) 

M 


Ampelomyces quisqualis, Trichoderma harzianum T39, Bacillus sp. F77, Cladosporium tenuissimum (Amsalem, 

2004) 


T. harzianum T39 (Fiamingo, 2007a) 

Trichoderma harzianum Rifai strain T-22 (Picton, 2003) 

Trichoderma harzianum T39 (Pertot, 2004) (Pertot, 2008) 

103


B 

O 

Powdery mildew on tomato, pathogen: Leveillula taurica, Oidium neolycopersici, Oidium lycopersicum, Oidium spp. 



Bacteria 


Pseudomonas fluorescens (Shashi, 2007) 

Bacteria 


Bacillus brevis (Seddon, 1999) 

Trichoderma harzianum (Shashi, 2007) 

Bcillus subtilis (Jacob, 2007) 

Rhizobacteria B101R, B212R, and A068R, (Silva, 2004) 

Serenade ; Pseudomonas strains (Laethauwer, 2006) 

M 


Acremonium alternatum (Kasselaki, 2006a, b) 

Lecanicillium lecanii (Mycotal) (Bardin, 2004) 

Lecanicillium muscarium (Bardin, 2008) 

Sporothrix flocculosa (Jarvis, 2007) 

Trichoderma spp. (Moreno-Velandia, 2007) (Velandia, 2007) 

Milsana (Seddon, 1999) 

MilsanaReg. (VP 1999)(Malathrakis, 2002) 

B 

Milsana (Trottin-Caudal, 2003) 

Malsana (Bardin, 2004) (Bardin, 2008) 

Milsana ; (Laethauwer, 2006) 

O 

Powdery mildew on pepper, pathogen: Podosphaera leucotricha 


Bacteria 




Bacteria 


M 

AQ10 (Ampelomyces quisqualis) (Tsror, 2004) 

Trichoderma harzianum (Gupta, 2005) 

Trichoderma harzianum T39; Ampelomyces quisqualis (Brand, 2002) 

Verticillium lecanii, Tilletiopsis minor (Haggag, 2008) 

B Milsana (Haggag, 2008) 

O Water extract of cattle manure compost, grape marc compost, , Kaligrin and Rifol (Tsror, 2004) 

104

Appendix 2 

Powdery mildew on cucurbits, pathogen: Podosphaera fusca 


Bacteria 

Bacillus brevis (Schmitt, 1999) 

Bacillus isolates (Koumaki, 2001) 

Brevibacillus brevis (Abd-El-Moneim, 2004) 

M 

B 

O 


Acremonium alternatum (Kasselaki, 2006a) 

Ampelomyces quisqualis (Kristkova, 2003) 

Ampelomyces quisqualis isolate M-10 (Benuzzi, 2006) 

Ampelomyces quisqualis, Verticillium lecanii, Sporothrix 

flocculosa (Dik, 1998) 

Cryptococcus laurentii and Aureobasidium pullulans (Lima, 

2002) 

PlantShield Trichoderma harzianum (Utkhede, 2006) 

Rhodotorula glutinis (Lima, 2002) 

T. harzianum T39 (Levy, 2004) 

Tilletiopsis washingtonensis (yeast) (El-Hafiz-Mohamed, 

1999) 

Verticillium lecanii; (Verhaar, 1999) 

fresh or dried milk (10%), pinolene 1%, calcium chloride (2%), 

tripotassium phosphate (1%) and a mixture of mineral oil 

(1%),sodium bicarbonate/sodium silicate (0.5%) (Casulli, 2002) 


Bacteria 

Bacillus spp (Romero, 2004a) 

Bacillus spp (Romero, 2004b) 

Bacillus subtilis (Abd-El-Moneim, 2004) (Gilardi, 2008) (Keinath, 2004) (Romero, 2007b) (Romero, 2007d) 


Brevibacillus brevis (Allan, 2007) (Konstantinidou-Doltsinis, 2002) (Schmitt, 2001) (White, 2001) 

Enterobacter cloacae (Georgieva, 2003) 

Xenorhabdus nematophilus (Shi, 2004) 


Acremonium alternatum, Ampelomyces quisqualis , Lecanicillium lecanii (Romero, 2003) 

Acremonium alternatum, Verticillium lecanii (Romero, 2007b) 

Ampelomyces quisqualis (Gilardi, 2008) (Rankovic, 1998) 

AQ10Reg. (Ampelomyces quisqualis) and MycotalReg. (Lecanicillium lecanii) (Romero, 2007b) 


Acremonium alternatum and Verticillium lecanii, (Romero, 2001) 

Lecanicillium longisporum (Kim, 2008) 

Lecanicillium spp. (Goettel, 2008) 

Meira geulakonigii (Sztejnberg, 2004) 

Paecilomyces fumosoroseus (Kavkova, 2005) 

Paecilomyces fumosoroseus; Verticillium lecanii (Kavkova, 2001) 

Pseudozyma flocculosa (Konstantinidou-Doltsinis, 2002) (Schmitt, 2001) 

Pseudozyma flocculosa, Ampelomyces quisqualis, Verticillium lecanii, Trichoderma harzianum (Dik, 2002) 

Saccharomyces cerevisiae (El-Gamal, 2003) 

Trichoderma harzianum (Abd-El-Moneim, 2004) (Elad, 2000) 

Trichoderma harzianum T39; Ampelomyces quisqualis AQ10 (Elad, 1998) 

Verticillium lecanii (Askary, 1998) (Verhaar, 1998) 

Ampelomyces quisqualis isolate M-10 (Benuzzi, 2006) 

Milsana (VP99) (Dik, 2002) (Schmitt, 2001) (White, 2001) 

Milsana (VP99) from Fallopia sachalinensis (Konstantinidou-Doltsinis, 2001) 

Fresh or dried milk (Casulli, 2002) 

gramicidin S; (Schmitt, 1999) 

lactoperoxidase system (Ravensberg, 2007) 

lipopeptide antibiotic neopeptins from Streptomyces sp. (Kim, 2007) 

lipopeptides (iturin and fengycin families of Bacillus subtilis) (Romero, 2007c) 

Lipopeptides of antagonistic strains of Bacillus subtilis (Romero, 2007a) 

oil formulations (Verhaar, 1999) 

Psyllobora bisoctonotata (Soylu, 2002) 

undiluted homogenised milk (Utkhede, 2006) 

105


Powdery mildew on various crops, pathogen: Oidium spp. Sphaerotheca spp., Erysiphe spp 



Bacteria 

Bacillus subtilis (Nofal, 2006) 

M 

B 

O 


Verticillium lecanIi, Tilletiopsis minor (Nofal, 2006) 

Bacteria 

Pseudomonas fluorescens (Vimala, 2006) 

P. fluorescens (Hooda, 2006) 


Acremonium spp., Ampelomyces spp., Penicillium spp., Cladosporium spp., Trichoderma spp., Bacillus spp., 

Pseudomonas spp., Bradyrhizobium spp., Brachybacterium spp., Curtobacterium spp., Cryptocoocus spp., 

Rhodosporidium spp (Mmbaga, 2008) 

Ampelomyces mycoparasites (Kiss, 2004) 

BCAs (Dhananjoy, 2008) 

BCAs (Eken, 2005) 

BCAs(Casey, 2007) 

Cladosporium cladosporioides, Cladosporium oxysporum, Drechslera hawaiensis,T richoderma viride (Sankar, 

2007b) 

Cladosporium oxysporum (Sankar, 2007a) 

Gliocladium roseum (Lahoz, 2004) 

Kyu-W63 (Koitabashi, 2005) 

Trichoderma viride, T. harzianum, Pseudomonas fluorescens, mixture of T. harzianum P. fluorescens (Hooda, 2006) 

Exudates from sclerotia of two Sclerotium rolfsii isolates (Pandey, 2007) 

Mycophagous Ladybird (Sutherland, 2005) 

Phyllactinia corylea (Krishnakumar, 2004) 

Psyllobora bisoctonotata (Muls.) (Soylu, 2002) 

Psyllobora vigintimaculata, (Sutherland, 2008; Sutherland, 2006) 

References 

Abd-El-Moneim, M. L. (2004). Integrated system to protect cucumber plants in greenhouses against diseases and pests under organic farming conditions. Egyptian-Journal-of-Agricultural- 

Research 82, 1-9. 

Alaphilippe, A. (2007). Effect of introduced epiphytic yeast on an insect pest (Cydia pomonella L.), on apple pathogens (Venturia inaequalis and Podosphaera leucotricha) and on the phylloplane 

chemical composition. Bulletin-OILB/SROP 30, 259-263. 

Alaphilippe, A. (2008). Effects of a biocontrol agent of apple powdery mildew (Podosphaera leucotricha) on the host plant and on non-target organisms: an insect pest (Cydia pomonella) and a 

pathogen (Venturia inaequalis). Biocontrol-Science-and-Technology 18, 121-138. 

Allan, E. J. (2007). Increased biocontrol efficacy of Brevibacillus brevis against cucurbit powdery mildew by combination with neem extracts. Bulletin-OILB/SROP 30, 401-404. 

Amaro, P. (2003). The good plant protection practice for grape vine is more concerned, in relation to IPM, with the risk of resistance than the safety and other side effects of pesticides. Bulletin 

OILB/SROP 26, 273-276. 

Amsalem, L. (2004). Efficacy of control agents on powdery mildew: a comparison between two populations. Bulletin-OILB/SROP 27, 309-313. 

Angeli, D. (2006a). Colonization of grapevine powdery mildew cleistothecia by the mycoparasite Ampelomyces quisqualis in Trentino, Italy. Bulletin-OILB/SROP 29, 89-92. 

Angeli, D. (2006b). Efficacy evaluation of integrated strategies for powdery and downy mildew control in organic viticulture. Bulletin-OILB/SROP 29, 51-56. 

Angeli, D. (2006c). Evaluation of new control agents against grapevine powdery mildew under greenhouse conditions. Bulletin-OILB/SROP 29, 83-87. 

Angeli, D. (2007a). Evaluation of new biological control agents against grapevine powdery mildew under greenhouse conditions. Bulletin-OILB/SROP 30, 37-42. 

Angeli, D. (2007b). Role of Ampelomyces quisqualis on grapevine powdery mildew in Trentino (northern Italy) vineyards. Bulletin-OILB/SROP 30, 245-248. 

Ari, M. E. (2004). Fungal diseases of grape. Crop-management-and-postharvest-handling-of-horticultural-products-Volume-IV:-Diseases-and-disorders-of-fruits-and-vegetables. 

106

Appendix 2 

Askary, H. (1998). Pathogenicity of the fungus Verticillium lecanii to aphids and powdery mildew. Biocontrol-Science-and-Technology 8, 23-32. 

Azarang, M. (2004). An integrated approach to simultaneously control insect pests, powdery mildew and seed borne fungal diseases in barley by bacterial seed treatment. Bulletin-OILB/SROP 

27, 57-62. 

Bardin, M. (2004). Compatibility of intervention to control grey mould, powdery mildew and whitefly on tomato, using three biological methods. Bulletin-OILB/SROP 27, 5-9. 

Bardin, M. (2008). Compatibility between biopesticides used to control grey mould, powdery mildew and whitefly on tomato. Biological-Control 46, 476-483. 

Barna, B. (2008). Effect of the Penicillium chrysogenum antifungal protein (PAF) on barley powdery mildew and wheat leaf rust pathogens. Journal-of-Basic-Microbiology 48, 516-520. 

Benuzzi, M. (2006). Efficacy of Ampelomyces quisqualis isolate M-10 (AQ 10Reg.) against powdery mildews (Erysiphaceae) on protected crops. Bulletin-OILB/SROP 29, 275-280. 

Brand, M. (2002). Effect of greenhouse climate on biocontrol of powdery mildew (Leveillula taurica) in sweet pepper and prospects for integrated disease management. Bulletin-OILB/SROP 25, 

69-72. 

Casey, C. (2007). IPM program successful in California greenhouse cut roses. California-Agriculture 61, 71-78. 

Casulli, F. (2002). Effectiveness of natural compounds in the suppression of the powdery mildew fungi Sphaerotheca fusca and Uncinula necator. Bulletin-OILB/SROP 25, 179-182. 

Crisp, P. (2006). An evaluation of biological and abiotic controls for grapevine powdery mildew. 1. Greenhouse studies. Australian-Journal-of-Grape-and-Wine-Research 12, 192-202. 

David, D. R. (2007). Development of biocontrol of powdery mildew diseases. Bulletin-OILB/SROP 30, 11-15. 

Dhananjoy, M. (2008). Natural weed-insect-microbes association in and around Sriniketan in Lateritic Belt of West Bengal: biocontrol implications. Journal-of-Plant-Protection-and- 

Environment 5, 34-37. 

Dik, A. J. (1998). Comparison of three biological control agents against cucumber powdery mildew (Sphaerotheca fuliginea) in semi-commercial-scale glasshouse trials. European-Journal-of- 

Plant-Pathology 104, 413-423. 

Dik, A. J. (2002). Combinations of control methods against powdery mildew diseases in glasshouse-grown vegetables and ornamentals. Bulletin-OILB/SROP 25, 5-8. 

Eken, C. (2005). A review of biological control of rose powdery mildew (Sphaerotheca pannosa var. rosae) by fungal antagonists. Acta-Horticulturae (690), 193-196. 

El-Gamal, N. G. (2003). Usage of some biotic and abiotic agents for induction of resistance to cucumber powdery mildew under plastic house conditions. Egyptian-Journal-of-Phytopathology 

31, 129-140. 

El-Hafiz-Mohamed, K. A. (1999). Induction and isolation of more efficient yeast mutants for the control of powdery mildew on cucumber. Annals-of-Agricultural-Science-Cairo 44, 283-292. 

Elad, Y. (1998). Management of powdery mildew and gray mould of cucumber by Trichoderma harzianum T39 and Ampelomyces quisqualis AQ10. BioControl- 43, 241-251. 

Elad, Y. (2000). Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop-Protection 19, 709-714. 

English-Loeb, G. (1999). Control of powdery mildew in wild and cultivated grapes by a tydeid mite. Biological-Control 14, 97-103. 

English-Loeb, G. (2006). Lack of trade-off between direct and indirect defence against grape powdery mildew in riverbank grape. Ecological-Entomology 31, 415-422. 

English-Loeb, G. (2007). Biological control of grape powdery mildew using mycophagous mites. Plant-Disease 91, 421-429. 

Fiamingo, F. (2007a). Effect of application time of control agents on Podosphaera aphanis and side effect of fungicides on biocontrol agents survival on strawberry leaves. Bulletin-OILB/SROP 

30, 433-436. 

Fiamingo, F. (2007b). First report of biocontrol activity of Pseudomonas reactans, pathogen of cultivated mushrooms, against strawberry powdery mildew in greenhouse trials. Bulletin- 

OILB/SROP 30, 33-36. 

Fuzi, I. (2003). Natural parasitism of Uncinula necator cleistothecia by Ampelomyces hyperparasites in the south-western vineyards of Hungary. Acta-Phytopathologica-et-Entomologica- 

Hungarica 38, 53-60. 

Georgieva, O. (2003). Biological control of powdery mildew and mildew cucumber with Enterobacter cloacae Jordan. Ecology-and-Future-Bulgarian-Journal-of-Ecological-Science 2, 32-34. 

Gilardi, G. (2008). Efficacy of the biocontrol agents Bacillus subtilis and Ampelomyces quisqualis applied in combination with fungicides against powdery mildew of zucchini. Journal-of-Plant- 

Diseases-and-Protection 115, 208-213. 

Goettel, M. S. (2008). Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases. Journal-of-Invertebrate-Pathology 98, 256-261. 

Gupta, S. K. (2005). Diseases of bell pepper under protected cultivation conditions and their management. Integrated-plant-disease-management-Challenging-problems-in-horticultural-andforest-pathology,-Solan,-India,-14-to-15-November-2003. 

Haggag, M. W. (2007). Biocontrol activity and molecular characterization of three Tilletiopsis spp. against grape powdery mildew. Plant-Protection-Bulletin-Taipei 49, 39-56. 

Haggag, W. M. (2008). Integrated management of powdery mildew and grey mould of greenhouse pepper in Egypt. Bulletin-OILB/SROP 32, 275. 

Harvey, N. G. (2006). Characterization of six polymorphic microsatellite loci from Ampelomyces quisqualis, intracellular mycoparasite and biocontrol agent of powdery mildew. 

Molecular Ecology Notes 6, 1188-1190. 

107


Haugaard, H. (2002). Mechanisms involved in control of Blumeria graminis f.sp. hordei in barley treated with mycelial extracts from cultured fungi. Plant-Pathology 51, 612-620. 

Hoffmann, P. (2007). The occurrence of cleistothecia of Erysiphe necator (grapevine powdery mildew) and their epidemiological significance in some vine-growing regions of Hungary. Acta- 

Phytopathologica-et-Entomologica-Hungarica 42, 9-16. 

Hooda, K. S. (2006). Impact of biocontrol agents on the health of garden pea (Pisum sativum) in Kumaon hills of Himalayas. Indian-Journal-of-Agricultural-Sciences 76, 573-574. 

Jacob, D. (2007). Biology and biological control of tomato powdery mildew (Oidium neolycopersici). Bulletin-OILB/SROP 30, 329-332. 

Jarvis, W. R. (2007). SporodexReg., fungal biocontrol for powdery mildew in greenhouse crops. Biological-control:-a-global-perspective. 

Kaine, G. (2003). The adoption of pest and disease management practices by grape growers in New Zealand. AERU-Discussion-Paper (150), 69-76. 

Kasselaki, A. M. (2006a). Control of Leveillula taurica in tomato by Acremonium alternatum is by induction of resistance, not hyperparasitism. European-Journal-of-Plant-Pathology 115, 263- 

267. 

Kasselaki, A. M. (2006b). Induction of resistance against tomato powdery mildew (Leveillula taurica) by Acremonium alternatum. Bulletin-OILB/SROP 29, 69-73. 

Kassemeyer, H. H. (1998). Induced resistance of grapevine - Perspectives of biological control of grapevine diseases. Bulletin-OILB/SROP 21, 43-45. 

Kavkova, M. (2001). Evaluation of mycoparasitic effect of Paecilomyces fumosoroseus and Verticillium lecanii on cucumber powdery mildew. Collection-of-Scientific-Papers,-Faculty-of- 

Agriculture-in-Ceske-Budejovice-Series-for-Crop-Sciences 18, 103-112. 

Kavkova, M. (2005). Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) as a potential mycoparasite on Sphaerotheca fuliginea (Ascomycotina: Erysiphales). Mycopathologia- 159, 

53-63. 

Keinath, A. P. (2004). Evaluation of fungicides for prevention and management of powdery mildew on watermelon. Crop-Protection 23, 35-42. 

Kim, J. (2002). Verlamelin, an antifungal compound produced by a mycoparasite, Acremonium strictum. Plant-Pathology-Journal 18, 102-105. 

Kim, J. (2008). Evaluation of Lecanicillium longisporum, VertalecReg. for simultaneous suppression of cotton aphid, Aphis gossypii, and cucumber powdery mildew, Sphaerotheca fuliginea, on 

potted cucumbers. Biological-Control 45, 404-409. 

Kim, Y. (2007). Biological evaluation of neopeptins isolated from a Streptomyces strain. Pest-Management-Science 63, 1208-1214. 

Kiss, L. (2004). Biology and biocontrol potential of Ampelomyces mycoparasites, natural antagonists of powdery mildew fungi. Biocontrol-Science-and-Technology 14, 635-651. 

Koike, M. (2004). Verticillium lecanii (Lecanicillium spp.) as epiphyte and its application to biological control of arthropod pests and diseases. Bulletin-OILB/SROP 27, 41-44. 

Koitabashi, M. (2002). Aromatic substances inhibiting wheat powdery mildew produced by a fungus detected with a new screening method for phylloplane fungi. Journal-of-General-Plant- 

Pathology 68, 183-188. 

Koitabashi, M. (2005). New biocontrol method for parsley powdery mildew by the antifungal volatiles-producing fungus Kyu-W63. Journal-of-General-Plant-Pathology 71, 280-284. 

Konstantinidou-Doltsinis, S. (2001). Efficacy of a new liquid formulation from Fallopia sachalinensis (Friedrich Schmidt Petrop.) Ronse Decraene as an inducer of resistance against powdery 

mildew in cucumber and grape. Bulletin-OILB/SROP 24, 221-224. 

Konstantinidou-Doltsinis, S. (2002). Combinations of biocontrol agents and MilsanaReg. against powdery mildew and grey mould in cucumber in Greece and the Netherlands. Bulletin- 

OILB/SROP 25, 171-174. 

Konstantinidou-Doltsinis, S. (2007). Control of powdery mildew of grape in Greece using SporodexReg. L and MilsanaReg. Journal-of-Plant-Diseases-and-Protection 114, 256-262. 

Koumaki, C. M. (2001). Control of cucumber powdery mildew (Sphaerotheca fuliginea) with bacterial and fungal antagonists. Bulletin-OILB/SROP 24, 375-378. 

Krishnakumar, R. (2004). Management of powdery mildew in mulberry using coccinellid beetles, Illeis cincta (Fabricius) and Illeis bistigmosa (Mulsant). Journal-of-Entomological-Research 

28, 241-246. 

Kristkova, E. (2003). Distribution of powdery mildew species on cucurbitaceous vegetables in the Czech Republic. Sodininkyste-ir-Darzininkyste 22, 31-41. 

Laethauwer, S. d. (2006). Evaluation of resistance inducing products for biological control of powdery mildew in tomato biocontrol of Oidium lycopersici in tomato by induced resistance. 

Parasitica- 62, 57-78. 

Lahoz, E. (2004). Induction of systemic resistance to Erysiphe orontii cast in tobacco by application on roots of an isolate of Gliocladium roseum Bainier. Journal-of-Phytopathology 152, 465- 

470. 

Lee, S. (2004). Biological control of powdery mildew by Q-fect WP (Ampelomyces quisqualis 94013) in various crops. Bulletin-OILB/SROP 27, 329-331. 

Levy, N. O. (2004). Integration of Trichoderma and soil solarization for disease management. Bulletin-OILB/SROP 27, 65-70. 

Lima, G. (2002). Survival and activity of biocontrol yeasts against powdery mildew of cucurbits in the field. Bulletin-OILB/SROP 25, 187-190. 

Linder, C., Viret, O., Spring, J. L., Droz, P., and Dupuis, D. (2006). Integrated and organic grape production: synthesis of seven experimental years. Viticulture integree et bio-organique: 

synthese de sept ans d'observations. 38, 235-243. 

108

Appendix 2 

Malathrakis, N. E. (2002). Efficacy of MilsanaReg. (VP 1999), a formulated plant extract from Reynoutria sachalinensis, against powdery mildew of tomato (Leveillula taurica). Bulletin- 

OILB/SROP 25, 175-178. 

Melidossian, H. S. (2005). Suppression of grapevine powdery mildew by a mycophagous mite. Plant-Disease 89, 1331-1338. 

Mmbaga, M. T. (2008). Identification of microorganisms for biological control of powdery mildew in Cornus florida. Biological-Control 44, 67-72. 

Moreno-Velandia, C. A. (2007). Biological control of foliar diseases in tomato greenhouse crop in Colombia: selection of antagonists and efficacy tests. Bulletin-OILB/SROP 30, 59-62. 

Nelson, H. E. (2005). Fusarium oxysporum f. sp. radicis-lycopersici can induce systemic resistance in barley against powdery mildew. Journal-of-Phytopathology 153, 366-370. 

Nofal, M. A. (2006). Integrated management of powdery mildew of mango in Egypt. Crop-Protection 25, 480-486. 

Pandey, M. K. (2007). Biochemical investigations of sclerotial exudates of Sclerotium rolfsii and their antifungal activity. Journal-of-Phytopathology 155, 84-89. 

Pertot, I. (2004). Use of biocontrol agents against powdery mildew in integrated strategies for reducing pesticide residues on strawberry: evaluation of efficacy and side effects. Bulletin- 

OILB/SROP 27, 109-113. 

Pertot, I. (2008). Integrating biocontrol agents in strawberry powdery mildew control strategies in high tunnel growing systems. Crop-Protection 27, 622-631. 

Picton, D. D. (2003). Control of powdery mildew on leaves and stems of gooseberry. HortTechnology- 13, 365-367. 

Prasad, D. (2005). Crop protection: management strategies. Crop-protection:-management-strategies. 

Rankovic, B. (1998). Conidia production of Ampelomyces quisqualis in culture using suspension method and artificial infection of powdery mildew pathogens (Erysiphe artemisiae and E. 

cichoracearum) by the mycoparasite. Zastita-Bilja 49, 77-84. 

Ravensberg, W. (2007). The lactoperoxidase system as a novel, natural fungicide for control of powdery mildew. Bulletin-OILB/SROP 30, 19-22. 

Robotic, V. (2002). Biological control of grapevine powdery mildew with Effective Microorganisms (EM). Bulletin-OILB/SROP 25, 191. 

Romero, D. (2001). Biological control of cucurbit powdery mildew by mycoparasitic fungi. Bulletin-OILB/SROP 24, 143-146. 

Romero, D. (2003). Effect of mycoparasitic fungi on the development of Sphaerotheca fusca in melon leaves. Mycological-Research 107, 64-71. 

Romero, D. (2004a). Effect of relative humidity on the efficacy of mycoparasitic fungi and antagonistic bacteria towards cucurbit powdery mildew. Bulletin-OILB/SROP 27, 301-304. 

Romero, D. (2004b). Isolation and evaluation of antagonistic bacteria towards the cucurbit powdery mildew fungus Podosphaera fusca. Applied-Microbiology-and-Biotechnology 64, 263-269. 

Romero, D. (2007a). Effect of lipopeptides of antagonistic strains of Bacillus subtilis on the morphology and ultrastructure of the cucurbit fungal pathogen Podosphaera fusca. Journal-of- 

Applied-Microbiology 103, 969-976. 

Romero, D. (2007b). Evaluation of biological control agents for managing cucurbit powdery mildew on greenhouse-grown melon. Plant-Pathology 56, 976-986. 

Romero, D. (2007c). The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Molecular-Plant-Microbe-Interactions 20, 

430-440. 

Romero, D. (2007d). Management of cucurbit powdery mildew on greenhouse-grown melons by different biological control strategies. Bulletin-OILB/SROP 30, 427-431. 

Sanin, S. S., Neklesa, N. P., and Strizhekozin, Y. A. (2008). Wheat protection from powdery mildew (supplement). Zashchita i Karantin Rastenii. 

Sankar, N. R. (2007a). Cladosporium oxysporum as a mycoparasite on Uncinula tectonae - a new record. Journal-of-Plant-Disease-Sciences 2, 182-183. 

Sankar, N. R. (2007b). Evaluation of teak phylloplane mycoflora for biocontrol of powdery mildew of teak caused by Uncinula tectonae. Journal-of-Plant-Disease-Sciences 2, 203-205. 

Schilder, A. M. C. (2002). Evaluation of environmentally friendly products for control of fungal diseases of grapes. 10th-International-Conference-on-Cultivation-Technique-and- 

Phytopathological-Problems-in-Organic-Fruit-Growing-and-Viticulture-Proceedings-of-a-conference,-Weinsberg,-Germany,-4-7-February-2002. 

Schmitt, A. (1999). Antifungal activity of gramicidin S and use of Bacillus brevis for control of Sphaerotheca fuliginea. Modern-fungicides-and-antifungal-compounds-II-12th-International- 

Reinhardsbrunn-Symposium,-Friedrichroda,-Thuringia,-Germany,-24th-29th-May-1998. 

Schmitt, A. (2001). Improved plant health by the combination of biological disease control methods. Bulletin-OILB/SROP 24, 29-32. 

Schmitt, A. (2002). Use of Reynoutria sachalinensis plant extracts, clay preparations and Brevibacillus brevis against fungal diseases of grape berries. 10th-International-Conference-on- 

Cultivation-Technique-and-Phytopathological-Problems-in-Organic-Fruit-Growing-and-Viticulture-Proceedings-of-a-conference,-Weinsberg,-Germany,-4-7-February-2002. 

Schweigkofler, W. (2006). Effects of fungicides on the germination of Ampelomyces quisqualis AQ10, a biological antagonist of the powdery mildew of the grapevine. Bulletin-OILB/SROP 29, 

79-82. 

Seddon, B. (1999). Integrated biological control of fungal plant pathogens using natural products. Modern-fungicides-and-antifungal-compounds-II-12th-International-Reinhardsbrunn- 

Symposium,-Friedrichroda,-Thuringia,-Germany,-24th-29th-May-1998. 

Shashi, K. (2007). Field efficacy of bioagents and fungicides against tomato (Lycopersicon esculentum Mill.) diseases. Environment-and-Ecology 25S, 921-924. 

109


Shen, D., Wei, S., Ji, Z., and Wu, W. (2008). Primary studies on the secondary metabolic products of strain A19 of actinomycetes. Journal of Northwest A & F University - Natural Science 

Edition 36, 173-178. 

Shi, Y. (2004). Studies on 0.25% aqueous solution of Xenorhabdus nematophilus for the control of cucumber powdery mildew. Plant-Protection 30, 79-81. 

Silva, H. S. A. (2004). Rhizobacterial induction of systemic resistance in tomato plants: non-specific protection and increase in enzyme activities. Biological-Control 29, 288-295. 

Simian, B. (2008). Inhibitory effect of phylloplane fungi on Erysiphe polygoni DC inciting powdery mildew disease of Trigonella foenum-graecum. Annals-of-Plant-Protection-Sciences 16, 

150-152. 

Sonali, V. (2005). Ampelomyces quisqualis Ces. - a mycoparasite of apple powdery mildew in western Himalayas. Indian-Phytopathology 58, 250-251. 

Soylu, S. (2002). Feeding of mycophagous ladybird, Psyllobora bisoctonotata (Muls.), on powdery mildew infested plants. Bulletin-OILB/SROP 25, 183-186. 

Sutherland, A. (2008). A preliminary predictive model for the consumption of powdery mildew by the obligate mycophage Psyllobora vigintimaculata (Coleoptera: Coccinellidae). Bulletin- 

OILB/SROP 32, 209-212. 

Sutherland, A. M. (2005). Effects of selected fungicides on a Mycophagous Ladybird (Coleoptera: Coccinellidae): ramifications for biological control of powdery mildew. Bulletin-OILB/SROP 

28, 253-256. 

Sutherland, A. M. (2006). Quantification of powdery mildew removal by the mycophagous beetle Psyllobora vigintimaculata (Coleoptera: Coccinellidae). Bulletin-OILB/SROP 29, 281-286. 

Szentivanyi, O. (2006). Paecilomyces farinosus destroys powdery mildew colonies in detached leaf cultures but not on whole plants. European-Journal-of-Plant-Pathology 115, 351-356. 

Sztejnberg, A. (2004). A new fungus with dual biocontrol capabilities: reducing the numbers of phytophagous mites and powdery mildew disease damage. Crop-Protection 23, 1125-1129. 

Tadesse, M. (2003). Bryophyte extracts with activity against plant pathogenic fungi. Sinet,-Ethiopian-Journal-of-Science 26, 55-62. 

Trottin-Caudal, Y. (2003). Efficiency of plant extract from Reynoutria sachalinensis (Milsana) to control powdery mildew on tomato (Oidium neolycopersici). Colloque-international-tomatesous-abri,-protection-integree-agriculture-biologique,-Avignon,-France,-17-18-et-19-septembre-2003. 

Tsror, L. (2004). Control of powdery mildew on organic pepper. Bulletin-OILB/SROP 27, 333-336. 

Utkhede, R. S. (2006). Reduction of powdery mildew caused by Podosphaera xanthii on greenhouse cucumber plants by foliar sprays of various biological and chemical agents. Journal-of- 

Horticultural-Science-and-Biotechnology 81, 23-26. 

Velandia, C. A. M. (2007). Survival in the phylloplane of Trichoderma koningii and biocontrol activity against tomato foliar pathogens. Bulletin-OILB/SROP 30, 557-561. 

Verhaar, M. A. (1998). Selection of Verticillium lecanii isolates with high potential for biocontrol of cucumber powdery mildew by means of components analysis at different humidity regimes. 

Biocontrol-Science-and-Technology 8, 465-477. 

Verhaar, M. A. (1999). Improvement of the efficacy of Verticillium lecanii used in biocontrol of Sphaerotheca fuliginea by addition of oil formulations. BioControl- 44, 73-87. 

Vimala, R. (2006). Enhancing resistance in bhendi to powdery mildew disease by foliar spray with fluorescent pseudomonads. International-Journal-of-Agricultural-Sciences 2, 549-556. 

White, D. (2001). Interaction of the biocontrol agent Brevibacillus brevis with other disease control methods. Bulletin-OILB/SROP 24, 229-232. 

Yigit, F. (2004). Integrated biological and chemical control of powdery mildew of barley caused by Blumeria graminis f.sp. hordei using rhizobacteria and triadimenol. Pakistan-Journal-of- 

Biological-Sciences 7, 1671-1675. 

Zulini, L. (2004). Biocontrol agents and their integration in organic viticulture in Trentino, Italy: characteristics and constrains. Bulletin-OILB/SROP 27, 49-52. 

110

Appendix 3. Inventory of biocontrol agents (M: microbials; B: botanicals; O: others) described in primary literature (1973-2008) 

for successful effect against the rust pathogens in laboratory experiments and field trials on selected crops 

Rust on wheat, oat, soybean, groundnut, bean 


Success in laboratory conditions (in vitro and/or in planta in controlled 

conditions) 

Bean – target pathogen = Uromyces appendiculatus 

Pantoea agglomerans B1 (Yuen et al., 2001) 

Stenotrophomonas maltophilia C3 (Yuen et al., 2001) 

Cladosporium tenuissimum (Assante et al., 2004) 

M 

B 

O 


Bacillus subtilis (Baker et al., 1985) 

Groundnut – target pathogen = Puccinia arachidis 

Pseudomonas fluorescens strain Pf1 (Meena et al., 2002) 

Groundnut – target pathogen = Puccinia arachidis 

Bacillus subtilis AF 1 (Manjula et al., 2004) 

Pseudomonas fluorescens strain Pf1 (Meena et al., 2000) (Meena et al., 2002) 

Acremonium obclavatum (Gowdu and Balasubramanian, 1993) 

Fusarium chlamydosporum (Mathivanan and Murugesan, 2000) (Mathivanan et 

al., 1998) 

Soybean – target pathogen = Phakopsora pachyrhizi 

Verticillium psalliotae, Verticillium lecanii (Saksirirat and Hoppe, 1990) 

(Saksirirat and Hoppe, 1991) 

Wheat, Oat – target pathogens = Puccinia recondite, P. coronata 

Pseudomonas putida strain BK8661 (Flaishman et al., 1996) 

Chaetomium globosum strain F0142 (Park et al., 2005b) 

Verticillium chlamydosporium (Leinhos and Buchenauer, 1992) 

endophytic fungi (Dingle and McGee, 2003) 

Fusaric acid from Fusarium oxysporum EF119 (Son et al., 2008) 


2,6-dichloro-isonicotinic acid (CGA 41396) (Dann and Deverall, 1995) 

111


Rust on other crops 



conditions) 

Chrysanthemum 

Verticillium lecanii (Whipps, 1993) 

M 

B 

O 

Coffee – target pathogens = Hemileia vastatrix 

Bacillus sp. (Haddad et al., 2006) 

Pseudomonas sp. (Maffia et al., 2005), variable effect (Haddad et al., 2006) 

Coffee – target pathogens = Hemileia vastatrix 

acibenzolar-S-methyl (ASM) (Patricio et al., 2008) 

Coffee – target pathogen = Hemileia vastatrix 

Bacillus lentimorbus (Shiomi et al., 2006) 

Bacillus cereus (Shiomi et al., 2006) 

Bacillus (Haddad et al., 2004) 

Cedecea davisae (Silva et al., 2008) 

Pseudomonas (Haddad et al., 2004) 

Acremonium (Haddad et al., 2004) 

Aspergillus (Haddad et al., 2004) 

Cladosporium (Haddad et al., 2004) 

Fusarium (Haddad et al., 2004) 

Penicillium (Haddad et al., 2004) 

Geranium – target pathogen = Puccinia pelargonii-zonalis 

Bacillus subtilis (Rytter et al., 1989) 

Safflower – target pathogen = Puccinia carthami 

Trichoderma viride and T. harzianum, Bacillus subtilis, B. cereus, B. thuringiensis, 

Pseudomonas fluorescens added alone and in combination (Tosi and Zazzerini, 

1994) 

Poplar – target pathogen = Melampsora ciliata 

Alternaria alternata and Cladosporium oxysporum (Sharma et al., 2002) 

Pine – target pathogens = Cronartium and Peridermium 

Cladosporium tenuissimum (Moricca et al., 2001) 

Scytalidium uredinicola (Moltzan et al., 2001) 

Plant-growth-promoting rhizobacteria (Enebak and Carey, 2004) 

112

Appendix 3 

References on biocontrol against the rust pathogens 

Assante, G., Maffi, D., Saracchi, M., Farina, G., Moricca, S., and Ragazzi, A. (2004). Histological studies on the mycoparasitism of Cladosporium tenuissimum on urediniospores of Uromyces appendiculatus. 

Mycological Research 108, 170-182. 

Baker, C. J., Stavely, J. R., and Mock, N. (1985). Biocontrol of bean rust by Bacillus-subtilis under field conditions. Plant Disease 69, 770-772. 

Dann, E. K., and Deverall, B. J. (1995). Effectiveness of systemic resistance in bean against foliar and soilborne pathogens as induced by biological and chemical means. Plant Pathology 44, 458-466. 

Dingle, J., and McGee, P. A. (2003). Some endophytic fungi reduce the density of pustules of Puccinia recondita f. sp tritici in wheat. Mycological Research 107, 310-316. 

Enebak, S. A., and Carey, W. A. (2004). Plant growth-promoting rhizobacteria may reduce fusiform rust infection in nursery-grown loblolly pine seedlings. Southern Journal of Applied Forestry 28, 185-188. 

Flaishman, M. A., Eyal, Z., Zilberstein, A., Voisard, C., and Haas, D. (1996). Suppression of Septoria tritici blotch and leaf rust of wheat by recombinant cyanide-producing strains of Pseudomonas putida. 

Molecular Plant-Microbe Interactions 9, 642-645. 

Gowdu, B. J., and Balasubramanian, R. (1993). Biocontrol potential of rust of groudnut by Acremonium-obclavatum. Canadian Journal of Botany-Revue Canadienne De Botanique 71, 639-643. 

Haddad, F., Maffia, L. A., Mizubuti, E. S., and Teixeira, H. (2006). Biological control of leaf rust in organically-grown coffee. Phytopathology 96, S44-S44. 

Haddad, F., Maffia, L. A., Mizubuti, E. S. G., and Romeiro, R. S. (2004). Biocontrol of coffee leaf rust with antagonists isolated from organic crops. Phytopathology 94, S37-S37. 

Leinhos, G. M. E., and Buchenauer, H. (1992). Inhibition of rust diseases of cereals by metabolic products of verticillium-chlamydosporium. Journal of Phytopathology-Phytopathologische Zeitschrift 136, 

177-193. 

Maffia, L., Haddad, F., Mizubuti, E., Teixeira, H., and Saraiva, R. (2005). Biocontrol of leaf rust in an organically-grown coffee planting. Phytopathology 95, S63-S64. 

Manjula, K., Kishore, G. K., and Podile, A. R. (2004). Whole cells of Bacillus subtilis AF 1 proved more effective than cell-free and chitinase-based formulations in biological control of citrus fruit rot and 

groundnut rust. Canadian Journal of Microbiology 50, 737-744. 

Mathivanan, N., Kabilan, V., and Murugesan, K. (1998). Purification, characterization, and antifungal activity of chitinase from Fusarium chlamydosporum, a mycoparasite to groundnut rust, Puccinia 

arachidis. Canadian Journal of Microbiology 44, 646-651. 

Mathivanan, N., and Murugesan, K. (2000). Fusarium chlamydosporum, a potent biocontrol agent to groundnut rust, Puccinia arachidis. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of 

Plant Diseases and Protection 107, 225-234. 

Meena, B., Radhajeyalakshmi, R., Marimuthu, T., Vidhyasekaran, P., Doraiswamy, S., and Velazhahan, R. (2000). Induction of pathogenesis-related proteins, phenolics and phenylalanine ammonia-lyase in 

groundnut by Pseudomonas fluorescens. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of Plant Diseases and Protection 107, 514-527. 

Meena, B., Radhajeyalakshmi, R., Marimuthu, T., Vidhyasekaran, P., and Velazhahan, R. (2002). Biological control of groundnut late leaf spot and rust by seed and foliar applications of a powder formulation 

of Pseudomonas fluorescens. Biocontrol Science and Technology 12, 195-204. 

Moltzan, B. D., Blenis, P. V., and Hiratsuka, Y. (2001). Temporal occurrence and impact of Scytalidium uredinicola, a mycoparasite of western gall rust. Canadian Journal of Plant Pathology-Revue 

Canadienne De Phytopathologie 23, 384-390. 

Moricca, S., Ragazzi, A., Mitchelson, K. R., and Assante, G. (2001). Antagonism of the two-needle pine stem rust fungi Cronartium flaccidum and Peridermium pini by Cladosporium tenuissimum in vitro 

and in planta. Phytopathology 91, 457-468. 

Park, J. H., Choi, G. J., Jang, K. S., Lim, H. K., Kim, H. T., Cho, K. Y., and Kim, J. C. (2005). Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. Fems 

Microbiology Letters 252, 309-313. 

Patricio, F. R. A., Almeida, I. M. G., Barros, B. C., Santos, A. S., and Frare, P. M. (2008). Effectiveness of acibenzolar-S-methyl, fungicides and antibiotics for the control of brown eye spot, bacterial blight, 

brown leaf spot and coffee rust in coffee. Annals of Applied Biology 152, 29-39. 

Rytter, J. L., Lukezic, F. L., Craig, R., and Moorman, G. W. (1989). Biological-control of geranium rust by Bacillus-subtilis. Phytopathology 79, 367-370. 

Saksirirat, W., and Hoppe, H. H. (1990). Verticillium-psalliotae, an effective mycoparasite of the soybean rust fungus Phakopsora-pachyrhizi syd. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz- 

Journal of Plant Diseases and Protection 97, 622-633. 

Saksirirat, W., and Hoppe, H. H. (1991). Secretion of extracellular enzymes by Verticillium-psalliotae treschow and Verticillium-lecanii (zimm) viegas during growth on uredospores of the soybean rust 

fungus (Phakopsora-pachyrhizi syd) in liquid cultures. Journal of Phytopathology-Phytopathologische Zeitschrift 131, 161-173. 

Sharma, S., Sharma, R. C., and Malhotra, R. (2002). Effect of the saprophytic fungi Alternaria alternata and Cladosporium oxysporum on germination, parasitism and viability of Melampsora ciliata 

urediniospores. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of Plant Diseases and Protection 109, 291-300. 

Shiomi, H. F., Silva, H. S. A., de Melo, I. S., Nunes, F. V., and Bettiol, W. (2006). Bioprospecting endophytic bacteria for biological control of coffee leaf rust. Scientia Agricola 63, 32-39. 

Silva, H. S. A., Terrasan, C. R. F., Tozzi, J. P. L., Melo, I. S., and Bettiol, W. (2008). Endophytic bacteria inducing enzymes correlated to the control of coffee leaf rust (Hemileia vastatrix). Tropical Plant 

Pathology 33, 49-54. 

113


Son, S. W., Kim, H. Y., Choi, G. J., Lim, H. K., Jang, K. S., Lee, S. O., Lee, S., Sung, N. D., and Kim, J. C. (2008). Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against 

Phytophthora infestans. Journal of Applied Microbiology 104, 692-698. 

Tosi, L., and Zazzerini, A. (1994). Evaluation of some fungi and bacteria for potential control of safflower rust. Journal of Phytopathology-Phytopathologische Zeitschrift 142, 131-140. 

Whipps, J. M. (1993). A review of white rust (Puccinia horiana Henn) disease on chrysanthemum and the potential for its biological control with Vertillium lecanii (Zimm) Viegas. Annals of Applied Biology 

122, 173-187. 

Yuen, G. Y., Steadman, J. R., Lindgren, D. T., Schaff, D., and Jochum, C. (2001). Bean rust biological control using bacterial agents. Crop Protection 20, 395-402. 

114


successful effect against the downy mildew / late blight pathogens in laboratory experiments and field trials on selected crops 

Potato (target pathogen = Phytophthora infestans) 


M 

Bacillus subtilis (Basu et al., 2001) 

Bacillus sp. isolate PB2 (Atia, 2005) effect < fungicides 

Pseudomonas fluorescens (Basu et al., 2001) 

Pseudomonas fluorescens isolate PPfl (Atia, 2005) effect < fungicides 

Pseudomonas (El-Sheikh et al., 2002) 

Gliocladium virens (Basu et al., 2001) 

Phytophthora cryptogea (Quintanilla, 2002) 

Trichoderma spp (Saikia and Azad, 1999) 

Trichoderma viride (Basu et al., 2001) (Basu and Srikanta, 2003) but no effect in other studies 

(Singh et al., 2001) (Arora, 2000) (Arora et al., 2006) 

little or no effect once in the field (good in lab): 

Acremonium strictum, Penicillium viridicatum and Penicillium aurantiogriseum (Arora, 2000) 

(Arora et al., 2006) 

Myrothecium verrucaria and Chaetomium brasiliense (Arora et al., 2006) 

B carvone (Quintanilla, 2002) 

O 

culture filtrates from Streptomyces padanus (Huang et al., 2007) 

negative effect: 

salicylic acid (Quintanilla, 2002) 


conditions) 

Serenade (Bacillus subtilis strain QST 713) (Stephan et al., 2005) (Olanya and 

Larkin, 2006) 

Bacillus subtilis B5 (Ajay and Sunaina, 2005) 

Bacillus, Pseudomonas, Rahnella, and Serratia (Daayf et al., 2003) 

Enterobacter cloacae (Slininger et al., 2007) 

Pseudomonas fluorescens (Slininger et al., 2007) 

Xenorhabdus bovienii (Eibel et al., 2004) 

Penicillium aurantiogriseum (Jindal et al., 1988) 

Penicillium viridicatum (Hemant et al., 2004) 

Trichodex (Stephan et al., 2005) 

Trichoderma viride (Hemant et al., 2004) 

Penicillium, Rhizoctonia and Trichoderma spp (Phukan and Baruah, 1991) 

various microorganisms (Stephan and Koch, 2002) 

carvone , thymol, pinochamphone, plumbagin (Quintanilla, 2002) 

extracts of Rheum rhabarbarum and Solidago canadensis (Stephan et al., 2005) 

oregano extract (Olanya and Larkin, 2006) 

Elot-Vis (Stephan et al., 2005) 

patatin J from potato tuber (Sharma et al., 2004) 

chitosan ElexaTM (Acar et al., 2008) 

cyclic lipopeptides from Pseudomonas: massetolide A (Tran Thi Thu, 2007) 

extracts from Pseudomonas fluorescens (Martinez and Osorio, 2007) 

115


Tomato (target pathogen = Phytophthora infestans) 


M 

Bacillus cereus (Silva et al., 2004) 

Burkholderia (Lozoya-Saldana et al., 2006), 

Pseudomonas (Lozoya-Saldana et al., 2006), 

Streptomyces (Lozoya-Saldana et al., 2006) 

B Nochi leaf extract (Vanitha and Ramachandram, 1999) 

O compost extracts (Zaller, 2006) 


conditions) 

Bacillus pumilus (Yan et al., 2002) 

Cellulomonas flavigena (Lourenco Junior et al., 2006) 

Pseudomonas fluorescens (Yan et al., 2002) (Ha et al., 2007) (Tran Thi Thu, 

2007) 

Streptomyces sp. AMG-P1 (Lee et al., 2005) 

Aspergillus sp., (Lourenco Junior et al., 2006) 

Candida sp. (Lourenco Junior et al., 2006) 

Cryptococcus sp. (Lourenco Junior et al., 2006) 

Fusarium oxysporum (Kim et al., 2007a) 

Penicillium sp. (Perez Mancia and Sanchez Garita, 2000) 

Trichoderma harzianum T39 (Ferrari et al., 2007) 

capsidiol (El-Wazeri and El-Sayed, 1977) 

Elot-vis (Ferrari et al., 2007) 

acibenzolar-S-methyl (Becktell et al., 2005) 

beta -amino butyric acid (Yan et al., 2002) 

Bion (benzothiadiazole) (Surviliene et al., 2003) 

bikaverin and fusaric acid (Son et al., 2008) 

cellulose (Perez Mancia and Sanchez Garita, 2000) 

chaetoviridin A (Park et al., 2005a) 


Chitoplant (Ferrari et al., 2007) 

extracts from actinomycete isolates (Mutitu et al., 2008) 

extracts from Bazzania trilobata and Diplophyllum albicans (Tadesse et al., 2003) 

extract from Gibberella zeae (Kim et al., 1995) 

phosphate (Becktell et al., 2005) 

116

Appendix 4 

Grapes (target pathogen = Plasmopara viticola) 

M 

B 

O 


Bacillus brevis (Schmitt et al., 2002) 

Bacillus subtilis (Serenade) (Schilder et al., 2002) 

Pseudomonas fluorescens (Rizoplan) (Kilimnik and Samoilov, 2000) (Rajeswari et al., 2008) 

Fusarium proliferatum (Falk et al., 1996) 

Trichoderma harzianum T39 (Vecchione et al., 2007) 

little or no effect once in the field: 

Bacillus licheniformis (Cravero et al., 2000) 

Biorange (Bacillus subtilis, Candida oleophila, Pseudomonas spp. and Streptomyces spp.) 

(Spera et al., 2003) 

Croplife (citrus and coconut extract) (Schilder et al., 2002) 

Plantfood (foliar fertilizer) (Schilder et al., 2002) 

Milsana (giant knotweed extract) (Schilder et al., 2002) (Schmitt et al., 2002) 

neem (Rajeswari et al., 2008) 

acylbenzolar-s methyl (Dagostin et al., 2006) 

chitosan (Elexa) (Schilder et al., 2002) 

Mycosin (Angeli et al., 2006) 

Pearl millet Pennisetum glaucum (target pathogen = Sclerospora graminicola) 


Bacillus pumilus strain INR7, strain SE34 (Raj et al., 2003) 

Bacillus subtilis (Raj et al., 2003) (Raj et al., 2005) 

Pseudomonas fluorescens (Umesha et al., 1998) (Latake and Kolase, 2007) 

M 

Gliocladium virens (Arun et al., 2004) (Raj et al., 2005) 

Trichoderma harzianum (Raj et al., 2005) (Latake and Kolase, 2007) 

Trichoderma lignorum (Raj et al., 2005) 

B 

O milk (cow) (Arun et al., 2004) 


conditions) 

Alternaria alternata (Musetti et al., 2004) 

Fusarium proliferatum (Bakshi et al., 2001) 

neem (Achimu and Schlosser, 1992) 

extract of giant knotweed (Schmitt, 1996) 

Alternaria alternata extracts (Musetti et al., 2006) 

EXP1, copper gluconate, salt of fatty acid, plant based alcohol extract (Dagostin et 

al., 2006) 


conditions) 

Pseudomonas fluorescens (Raj et al., 2004) 

Aspergillus flavus, Trichoderma harzianum and T. viride (Surender et al., 2005) 

117


Other Vegetables and fruits 


Cauliflower and other crucifers (target pathogen = Peronospora parasitica) 

M 

B 

Bion (Pratibha et al., 2004) 

O 

phosphonate (Kofoet and Fischer, 2007) 

Lettuce (Bremia lactucae) 

M 

B 

phosphonate (Kofoet and Fischer, 2007) 

O Trichodermin (Borovko, 2005) 

Pimonex, Timorex and also Alkalin potassium+silicon (Robak and Ostrowska, 2006) 

Melon / cucumber (target pathogen = Pseudoperonospora cubensis) 

M 

B 

O phosphonate (Kofoet and Fischer, 2007) 

Miscellaneous 

Azotobacter slight effect against Peronospora arborescens on opium poppy (Chakrabarti and 

M 

Yadav, 1991) 

B 

O phosphonate against Peronospora destructor on Allium (Kofoet and Fischer, 2007) 


conditions) 

Pseudomonas sp. XBC-PS (Li et al., 2007) 

Trichoderma harzianum (Pratibha et al., 2004) 

Bion (Gawande and Sharma, 2003) 

actinomycete (Shu and An, 2004) 

Bacillus strains, Z-X-3 and Z-X-10 (Li et al., 2003) 

attenuated cucumber mosaic cucumovirus (Qin et al., 1992) 


compost extracts (Winterscheidt et al., 1990) 

Cladosporium chlorocephalum against Peronospora arborescens (Chaurasia and 

Dayal, 1985) (Nalini and Rai, 1988) 

DL- beta -amino-n-butyric acid (BABA) against Plasmopara helianthi (Tosi and 

Zazzerini, 2000) 

118

Appendix 4 

References on biocontrol against the downy mildew / late blight pathogens 

Acar, O., Aki, C., and Erdugan, H. (2008). Fungal and bacterial diseases control with ElexaTM plant booster. Fresenius Environmental Bulletin 17, 797-802. 

Achimu, P., and Schlosser, E. (1992). Effect of neem seed extracts (Azadirachta indica A. Juss) against downy mildew (Plasmopara viticola) of grapevine. Mededelingen van de Faculteit 

Landbouwwetenschappen, Universiteit Gent 57, 423-431. 

Ajay, S., and Sunaina, V. (2005). Direct inhibition of Phytophthora infestans, the causal organism of late blight of potato by Bacillus antagonists. Potato Journal 32, 179-180. 

Angeli, D., Maines, L., and Pertot, I. (2006). Efficacy evaluation of integrated strategies for powdery and downy mildew control in organic viticulture. Bulletin OILB/SROP 29, 51-56. 

Arora, R. K. (2000). Biocontrol of potato late blight. In "Potato, global research & development. Proceedings of the Global Conference on Potato, New Delhi, India, 6-11 December, 1999: Volume 1", pp. 

620-623. 

Arora, R. K., Garg, I. D., and Khurana, S. M. P. (2006). Achievements in biological control of diseases of potato with antagonistic organisms in Central Potato Research Institute, Shimla. In "Current status of 

biological control of plant diseases using antagonistic organisms in India. Proceedings of the group meeting on antagonistic organisms in plant disease management held at Project Directorate of 

Biological Control, Bangalore, India on 10-11th July 2003", pp. 236-243. 

Arun, K., Bhansali, R. R., and Mali, P. C. (2004). Raw cow's milk and Gliocladium virens induced protection against downy mildew of pearl millet. International Sorghum and Millets Newsletter 45, 64-65. 

Atia, M. M. M. (2005). Biological and chemical control of potato late blight disease. Annals of Agricultural Science, Moshtohor 43, 1401-1421. 

Bakshi, S., Sztejnberg, A., and Yarden, O. (2001). Isolation and characterization of a cold-tolerant strain of Fusarium proliferatum, a biocontrol agent of grape downy mildew. Phytopathology 91, 1062-1068. 

Basu, A., Konar, A., Mukhopadhyay, S. K., and Chettri, M. (2001). Biological management of late blight of potato using talc-based formulations of antagonists. Journal of the Indian Potato Association 28, 

80-81. 

Basu, A., and Srikanta, D. (2003). Integrated management of potato (Solanum tuberosum) diseases in Hooghly area of West Bengal. Indian Journal of Agricultural Sciences 73, 649-651. 

Becktell, M. C., Daughtrey, M. L., and Fry, W. E. (2005). Epidemiology and management of petunia and tomato late blight in the greenhouse. Plant Disease 89, 1000-1008. 

Borovko, L. (2005). Application of biological preparations to spring oilseed rape under ecological conditions. Rosliny Oleiste 26, 361-368. 

Chakrabarti, D. K., and Yadav, A. L. (1991). Effect of Azotobacter species on incidence of downy mildew (Peronospora arborescens) and growth and yield of opium poppy (Papaver somniferum). Indian 

Journal of Agricultural Sciences 61, 287-288. 

Chaurasia, S. N. P., and Dayal, R. (1985). Mycoparastitic nature of Cladosporium chlorocephalum with Peronospora arborescens causing downy mildew of opium. Indian Phytopathology 38, 467-470. 

Cravero, S., Bosca, P., Ferrari, D., and Scapin, I. (2000). Evaluation of the effectiveness of traditional and new compounds against grapevine downy mildew. In "Atti, Giornate fitopatologiche, Perugia, 16-20 

aprile, 2000, Volume 2", pp. 155-162. 

Daayf, F., Adam, L., and Fernando, W. G. D. (2003). Comparative screening of bacteria for biological control of potato late blight (strain US-8), using in-vitro, detached-leaves, and whole-plant testing 

systems. Canadian Journal of Plant Pathology 25, 276-284. 

Dagostin, S., Ferrari, A., and Pertot, I. (2006). Efficacy evaluation of biocontrol agents against downy mildew for copper replacement in organic grapevine production in Europe. Bulletin OILB/SROP 29, 15- 

21. 

Eibel, P., Schmitt, A., Stephan, D., Carvalho, S. M., Seddon, B., and Koch, E. (2004). Strategies to provide integrated biological control of late blight of potato to replace copper for sustainable organic 

agriculture production. Bulletin OILB/SROP 27, 79. 

El-Sheikh, M. A., El-Korany, A. E., and Shaat, M. M. (2002). Screening for bacteria antagonistic to Phytophthora infestans for the organic farming of potato. Alexandria Journal of Agricultural Research 47, 

169-178. 

El-Wazeri, S. M., and El-Sayed, S. A. (1977). Experimental control of soreshin disease in cotton and late blight in tomato by a natural antibiotic, capsidiol, that was synthesized by pepper fruits. Egyptian 

Journal of Horticulture 4, 151-156. 

Falk, S. P., Pearson, R. C., Gadoury, D. M., Seem, R. C., and Sztejnberg, A. (1996). Fusarium proliferatum as a biocontrol agent against grape downy mildew. Phytopathology 86, 1010-1017. 

Ferrari, A., Dubeshko, S., Vintel, H., David, D. R., and Elad, Y. (2007). Integration of biocontrol agents and natural products against tomato late blight. Bulletin OILB/SROP 30, 437-440. 

Gawande, S., and Sharma, P. (2003). Changes in host enzyme activity due to induction of resistance against downy mildew in cauliflower. Annals of Agricultural Research 24, 322-331. 

Ha, T., Ficke, A., Asiimwe, T., Hofte, M., and Raaijmakers, J. M. (2007). Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by 

Pseudomonas fluorescens. New Phytologist 175, 731-742. 

Hemant, G., Singh, B. P., and Jitendra, M. (2004). Biological control of late blight of potato. Journal of the Indian Potato Association 31, 39-42. 

Huang, J., Shih, H., Huang, H., and Chung, W. (2007). Effects of nutrients on production of fungichromin by Streptomyces padanus PMS-702 and efficacy of control of Phytophthora infestans. Canadian 


Jindal, K. K., Singh, H., and Madhu, M. (1988). Biological control of Phytophthora infestans on potato. Indian Journal of Plant Pathology 6, 59-62. 

119


Kilimnik, A. N., and Samoilov, Y. K. (2000). Approaches to control downy mildew. Zashchita i Karantin Rastenii, 29. 

Kim, B., Kim, K., Lee, J., Lee, Y., and Cho, K. (1995). Isolation and purification of several substances produced by Fusarium graminearum and their antimicrobial activities. Korean Journal of Plant 

Pathology 11, 158-164. 

Kim, H. Y., Choi, G. J., Lee, H. B., Lee, S. W., Lim, H. K., Jang, K. S., Son, S. W., Lee, S. O., Cho, K. Y., Sung, N. D., and Kim, J. C. (2007). Some fungal endophytes from vegetable crops and their antioomycete 

activities against tomato late blight. Letters in Applied Microbiology 44, 332-337. 

Kofoet, A., and Fischer, K. (2007). Evaluation of plant resistance improvers to control Peronospora destructor, P. parasitica, Bremia lactucae and Pseudoperonospora cubensis. Journal of Plant Diseases and 

Protection 114, 54-61. 

Latake, S. B., and Kolase, S. V. (2007). Screening of bioagents for control of downy mildew of pearl millet. International Journal of Agricultural Sciences 3, 32-35. 

Lee, H. B., Kim, Y., Kim, J. C., Choi, G. J., Park, S. H., Kim, C. J., and Jung, H. S. (2005). Activity of some aminoglycoside antibiotics against true fungi, Phytophthora and Pythium species. Journal of 


Li, J., Feng, S., and Xiao, J. (2007). The biological control effect of endophytic Pseudomonas XBC-PS from pakchoi. China Vegetables, 21-23. 

Li, X., Zhang, D., Yang, W., Dong, L., and Liu, D. (2003). A study on the effect of Bacillus on downy mildew of cucumber. Plant Protection 29, 25-27. 

Lourenco Junior, V., Maffia, L. A., Romeiro, R. d. S., and Mizubuti, E. S. G. (2006). Biocontrol of tomato late blight with the combination of epiphytic antagonists and rhizobacteria. Biological Control 38, 

331-340. 

Lozoya-Saldana, H., Coyote-Palma, M. H., Ferrera-Cerrato, R., and Lara-Hernandez, M. E. (2006). Microbial antagonism against Phytophthora infestans (Mont) de Bary. Agrociencia (Montecillo) 40, 491- 

499. 

Martinez, E. P., and Osorio, J. A. (2007). Preliminary studies for the production of an active biosurfactant against Phytophthora infestans (Mont.) de Bary. Revista Corpoica - Ciencia y Tecnologia 

Agropecuarias 8, 5-16. 

Musetti, R., Stringher, L., Vecchione, A., Borselli, S., and Pertot, I. (2004). Biocontrol agents against downy mildew of grape: an ultrastructural study. Bulletin OILB/SROP 27, 299. 

Musetti, R., Vecchione, A., Stringher, L., Borselli, S., Zulini, L., Marzani, C., D'Ambrosio, M., Toppi, L. S. d., and Pertot, I. (2006). Inhibition of sporulation and ultrastructural alterations of grapevine downy 

mildew by the endophytic fungus Alternaria alternata. Phytopathology 96, 689-698. 

Mutitu, E. W., Muiru, W. M., and Mukunya, D. M. (2008). Evaluation of antibiotic metabolites from actinomycete isolates for the control of late blight of tomatoes under greenhouse conditions. Asian Journal 

of Plant Sciences 7, 284-290. 

Nalini, N., and Rai, B. (1988). Cladosporium cladosporioides as a mycoparasite of Peronospora arborescens. Acta Botanica Indica 16, 257-259. 

Olanya, O. M., and Larkin, R. P. (2006). Efficacy of essential oils and biopesticides on Phytophthora infestans suppression in laboratory and growth chamber studies. Biocontrol Science and Technology 16, 

901-917. 

Park, J., Choi, G., Jang, K., Lim, H., Kim, H., Cho, K., and Kim, J. (2005). Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. FEMS Microbiology 

Letters 252, 309-313. 

Perez Mancia, J. E., and Sanchez Garita, V. (2000). Effect of the substrate cellulose and glucan on antagonists of Phytophthora infestans on tomato. Manejo Integrado de Plagas, 45-53. 

Phukan, S. N., and Baruah, C. K. (1991). Effect of tuber surface microflora on the incidence of late blight fungus Phytophthora infestans. Indian Journal of Ecology 18, 32-35. 

Pratibha, S., Sain, S. K., Sindhu, M., and Kadu, L. N. (2004). Integrated use of CGA245704 and Trichoderma harzianum on downy mildew supression and enzymatic activity in cauliflower. Annals of 

Agricultural Research 25, 129-134. 

Qin, B. Y., Zhang, X. H., Wu, G. S., and Tien, P. (1992). Plant resistance to fungal diseases induced by the infection of cucumber mosaic virus attenuated by satellite RNA. Annals of Applied Biology 120, 

361-366. 

Quintanilla, P. (2002). Biological control in potato and tomato to enhance resistance to plant pathogens - especially against Phytophthora infestans in potato. In "Acta Universitatis Agriculturae Sueciae - 

Agraria", pp. 88 pp. 

Raj, S. N., Chaluvaraju, G., Amruthesh, K. N., Shetty, H. S., Reddy, M. S., and Kloepper, J. W. (2003). Induction of growth promotion and resistance against downy mildew on pearl millet (Pennisetum 

glaucum) by rhizobacteria. Plant Disease 87, 380-384. 

Raj, S. N., Shetty, N. P., and Shetty, H. S. (2004). Seed bio-priming with Pseudomonas fluorescens isolates enhances growth of pearl millet plants and induces resistance against downy mildew. International 

Journal of Pest Management 50, 41-48. 

Raj, S. N., Shetty, N. P., and Shetty, H. S. (2005). Synergistic effects of Trichoshield on enhancement of growth and resistance to downy mildew in pearl millet. BioControl 50, 493-509. 

Rajeswari, E., Chitra, K., Seetharaman, K., and Sankaralingam, V. (2008). Exploiting medicinal plants and phylloplane microflora for the management of grapevine downy mildew. Archives of 

Phytopathology and Plant Protection 41, 213-220. 

120

Appendix 4 

Robak, J., and Ostrowska, A. (2006). The most important disease of small area vegetable (minor crops) cultivation and potential possibility of their control. Progress in Plant Protection 46, 114-120. 

Saikia, R., and Azad, P. (1999). In vivo effect of some Trichoderma spp. and Dithane M-45 against late blight of potato. Neo Botanica 7, 89-91. 

Schilder, A. M. C., Gillett, J. M., Sysak, R. W., and Wise, J. C. (2002). Evaluation of environmentally friendly products for control of fungal diseases of grapes. In "10th International Conference on 

Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing and Viticulture. Proceedings of a conference, Weinsberg, Germany, 4-7 February 2002", pp. 163-167. 

Schmitt, A. (1996). Plant extracts as pest and disease control agents. In "Atti convegno internazionale: Coltivazione e miglioramento di piante officinali, Trento, Italy, 2-3 giugno 1994." pp. 265-272. 

Schmitt, A., Kunz, S., Nandi, S., Seddon, B., and Ernst, A. (2002). Use of Reynoutria sachalinensis plant extracts, clay preparations and Brevibacillus brevis against fungal diseases of grape berries. In "10th 

International Conference on Cultivation Technique and Phytopathological Problems in Organic Fruit-Growing and Viticulture. Proceedings of a conference, Weinsberg, Germany, 4-7 February 2002", 

pp. 146-151. 

Sharma, N., Gruszewski, H. A., Park, S. W., Holm, D. G., and Vivanco, J. M. (2004). Purification of an isoform of patatin with antimicrobial activity against Phytophthora infestans. Plant Physiology and 

Biochemistry 42, 647-655. 

Shu, X., and An, D. (2004). Studies on the effect of zuelaemycin producing actinomycetes strain S-5120 on downy mildew of cucumber. Acta Botanica Boreali-Occidentalia Sinica 24, 2118-2122. 

Silva, H. S. A., Romeiro, R. S., Carrer Filho, R., Pereira, J. L. A., Mizubuti, E. S. G., and Mounteer, A. (2004). Induction of systemic resistance by Bacillus cereus against tomato foliar diseases under field 

conditions. Journal of Phytopathology 152, 371-375. 

Singh, B. P., Singh, P. H., Jhilmil, G., and Lokendra, S. (2001). Integrated management of late blight under Shimla hills. Journal of the Indian Potato Association 28, 84-85. 

Slininger, P. J., Schisler, D. A., Ericsson, L. D., Brandt, T. L., Frazier, M. J., Woodell, L. K., Olsen, N. L., and Kleinkopf, G. E. (2007). Biological control of post-harvest late blight of potatoes. Biocontrol 

Science and Technology 17, 647-663. 

Son, S. W., Kim, H. Y., Choi, G. J., Lim, H. K., Jang, K. S., Lee, S. O., Lee, S., Sung, N. D., and Kim, J. C. (2008). Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against 

Phytophthora infestans. Journal of Applied Microbiology 104, 692-698. 

Spera, G., Torre, A. l., and Alegi, S. (2003). Organic viticulture: efficacy evaluation of different fungicides against Plasmopara viticola. Communications in Agricultural and Applied Biological Sciences 68, 

837-847. 

Stephan, D., and Koch, E. (2002). Screening of plant extracts, micro-organisms and commercial preparations for biocontrol of Phytophthora infestans on detached potato leaves. Bulletin OILB/SROP 25, 391- 

394. 

Stephan, D., Schmitt, A., Carvalho, S. M., Seddon, B., and Koch, E. (2005). Evaluation of biocontrol preparations and plant extracts for the control of Phytophthora infestans on potato leaves. European 


Surender, K., Sushil, S., Sharma, B. K., and Thakur, D. P. (2005). Evaluation of mycoflora for antagonism against Sclerospora graminicola causing downy mildew of pearl millet. Environment and Ecology 

23S, 523-526. 

Surviliene, E., Brazaityte, A., and Sidlauskiene, A. (2003). Effect of benzotiadiazole on phytopathological and physiological processes in tomato. Zemes ukio Mokslai, 34-40. 

Tadesse, M., Steiner, U., Hindorf, H., and Dehne, H. W. (2003). Bryophyte extracts with activity against plant pathogenic fungi. Sinet, Ethiopian Journal of Science 26, 55-62. 

Tosi, L., and Zazzerini, A. (2000). Interactions between Plasmopara helianthi, Glomus mosseae and two plant activators in sunflower plants. European Journal of Plant Pathology 106, 735-744. 

Tran Thi Thu, H. (2007). Interactions between biosurfactant-producing Pseudomonas and Phytophthora species. In "Interactions between biosurfactant-producing Pseudomonas and Phytophthora species", pp. 

133 pp. 

Umesha, S., Dharmesh, S. M., Shetty, S. A., Krishnappa, M., and Shetty, H. S. (1998). Biocontrol of downy mildew disease of pearl millet using Pseudomonas fluorescens. Crop Protection 17, 387-392. 

Vanitha, S., and Ramachandram, K. (1999). Management of late blight disease of tomato with selected fungicides and plant products. South Indian Horticulture 47, 306-307. 

Vecchione, A., Silvia, D., Zulini, L., and Pertot, I. (2007). Trichoderma harzianum T39 activity against Plasmopara viticola. Bulletin OILB/SROP 30, 143-146. 

Winterscheidt, H., Minassian, V., and Weltzien, H. C. (1990). Studies on biological control of cucumber downy mildew - (Pseudoperonospora cubensis (Berk. et Curt.) Rost) - with compost extracts. Gesunde 

Pflanzen 42, 235-238. 

Yan, Z. N., Reddy, M. S., Ryu, C. M., McInroy, J. A., Wilson, M., and Kloepper, J. W. (2002). Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. 


Zaller, J. G. (2006). Foliar spraying of vermicompost extracts: effects on fruit quality and indications of late-blight suppression of field-grown tomatoes. Biological Agriculture & Horticulture 24, 165-180. 

121


successful effect against Monilinia in laboratory experiments and field trials on selected crops 

Apple (target pathogens = Monilinia fructigena; M. laxa) 


M 

Apricot (target pathogen = Monilinia laxa) 


M 

bacteria 

Burkholderia gladii OSU 7 (Altindag et al., 2006) (Esitken et al., 2005) 

Bacillus OSU-142 and Pseudomonas BA-8 (Esitken et al., 2005) 

Plum (target pathogen = Monilinia laxa) 


M 


conditions) 

Aureobasidium pullulans, Epicoccum purpurascens, Sordaria fimicola and 

Trichoderma polysporum (Falconi and Mendgen, 1994) 

Metschnikowia pulcherrima and (Spadaro et al., 2002), (Migheli et al., 1997) 

Pseudomonas syringae (Migheli et al., 1997) 

(M laxa) 

Pantoea agglomerans strain EPS125 (Bonaterra et al., 2004) 


conditions) 

bacteria 


(M fructicola) 

Bacillus subtillis strain B3 (Pusey and Wilson, 1984) 

fungi, yeasts 

Metschnikowia pulcherrima (Grebenisan et al., 2006) (Grebenisan et al., 2008) 


conditions) 

bacteria 


Epicoccum nigrum (Larena et al., 2001) 

Penicillium frequentans (Cal et al., 2002) 


Bacillus subtillis strain B3 (Pusey and Wilson, 1984) 

remark: no B or O for any of the crops 

122

Appendix 5 

Cherry (target pathogens = Monilia fructicola, M. laxa, M. fructigena) 


M 

B 

O 

bacteria 

(M laxa) 

Serenade (Bacillus subtilis QRD137) (Haseli and Weibel, 2002), 

fungi, yeasts 


Cryptococcus laurentii (Tian et al., 2004a) 

Epicoccum purpurascens (E. nigrum) and Gliocladium roseum (Wittig et al., 1997) 

(M laxa) 

Aureobasidium pullulans isolates 533 and 547 (Schena et al., 2003) 

(M laxa) 

Trilogy (azadirachtin-free Neemoil) (Haseli and Weibel, 2002) 

(M laxa) 

lime sulphur (calcium polysulfide) (Haseli and Weibel, 2002) 

Blueberry (target pathogen = Monilinia vaccinii-corymbos) 


M 

B 

O 

bacteria 

Serenade (Bacillus subtilis QRD137) (Ngugi et al., 2005) (Dedej et al., 2004) (Scherm and Stanaland, 

2001) (Schilder et al., 2006) 


conditions) 

bacteria 


Bacillus subtilis (15 isolates) (Utkhede and Sholberg, 1986) 

Burkholderia cepacia, Bacillus subtilis (Fan et al., 2001) 

(M laxa) 

Risoplan (Pseudomonas fluorescens), Gaupsin (Pseudomonas aureofaciens = P. 

chlororaphis) (Shevchuk, 2006) 


fungi, yeasts 


Candida guilliermondii, Kloeckera apiculata, Debaryomyces hansenii (Fan et al., 

2001) 

Cryptococcus infirmo-miniatus (Spotts et al., 2002) 

Cryptococcus laurentii (Wang and Tian, 2007) (Qin and Tian, 2005) (Qin et al., 

2006) 

(M laxa + M fructigena) 

Trichodex (Trichoderma harzianum) (Cardei, 2001) 


conditions) 

bacteria 

BlightBan (Pseudomonas fluorescens A506) (Scherm et al., 2004) 

Serenade (Bacillus subtilis QRD137) (Scherm et al., 2004) (Thornton et al., 2008) 

Pantoea agglomerans C9-1Sv (Thornton et al., 2008) 

fungi, yeasts 

Gliocladium roseum H47 (Thornton et al., 2008) 

123


Peach / Nectarine (target pathogens = Monilia fructicola, M. laxa, M. fructigena) 


M 

B ( 

bacteria 


Pseudomonas corrugata and P. cepacia; Bacillus subtilis strain B3 (Smilanick et al., 1993) 

fungi, yeasts 

Epicoccum nigrum (Mari et al., 2007) 

(M laxa) 

Epicoccum nigrum (Cal et al., 2004) (Foschi et al., 1995) (Larena et al., 2005) (Madrigal et al., 

1994) (Melgarejo et al., 1986) 

Penicillium frequentans (Cal et al., 1990) (Melgarejo et al., 1986) (Pascual et al., 2000) 

Penicillium purpurogenum (Melgarejo et al., 1986) 

O Sodium bicarbonate enhances effect of Aspire (Candida oleophila) (Droby et al., 2003) 


conditions) 

bacteria 


Rizo-N (Bacillus subtilis) (El-Sheikh Aly et al., 2000) 

Bacillus amyloliquefaciens C06 (Zhou et al., 2008) 

Bacillus subtillis (Gueldner et al., 1988) 

Bacillus subtillis strain B3 (Pusey et al., 1986) (Pusey et al., 1988) (Pusey, 1989) 

(Pusey and Wilson, 1984) 

Pantoea agglomerans strain IC1270 (Ritte et al., 2002) 

Pseudomonas syringae NSA-6 (Zhou et al., 1999) 

(M laxa) 

Pantoea agglomerans strain EPS125 (Bonaterra et al., 2003) (Bonaterra et al., 

2004) 

fungi, yeasts 


Candida sp(Karabulut et al., 2002) 

Cryptococcus laurentii (Yao and Tian, 2005) 

Debaryomyces hansenii (Stevens et al., 1997) (Stevens et al., 1998) 

Kloeckera apiculata yeast (Karabulut and Baykal, 2003) (McLaughlin et al., 1992) 

Muscodor albus (Mercier and Jimenez, 2004) (Schnabel and Mercier, 2006) 

Pichia membranaefaciens (Xu et al., 2008) 

Trichoderma atroviride (2 isolates), T viride & Rhodotorula sp (Hong et al., 1998) 

Plant-guard (T. harzianum) (El-Sheikh Aly et al., 2000) 

(M laxa) 

Penicillium purpurogenum (Foschi et al., 1995) (Larena and Melgarejo, 1996) 

Penicillium frequentans (Foschi et al., 1995) 

Trichoderma koningii (Foschi et al., 1995) 

Extract from Bacillus subtillis (McKeen et al., 1986) 

Iturin peptides from Bacillus subtillis (Gueldner et al., 1988) 

Sodium bicarbonate (Wisniewski et al., 2001); enhances effect of Aspire (Candida 

oleophila) (Droby et al., 2003) 

124

Appendix 5 

Successful inhibition in vitro (target pathogen = B. cinerea) 

Bacteria 

Pseudomonas syringae pv. morsprunorum BA35, Erwinia herbicola C9- (Voland et al., 1999) 

Serratia plymuthica, isolate EF-5 (Frommel et al., 1991) 

M 


Penicillium frequentans (Cal and Melgarejo, 1994) (Melgarejo et al., 1985) 

Aspergillus flavus, Epicoccum nigrum, Penicillium chrysogenum and P. purpurogenum (Melgarejo et al., 1985) 

B 

O Thiolutin from Streptomyces luteosporeus (Deb and Dutta, 1984) 

References on biocontrol against Monilia 

Altindag, M., Sahin, M., Esitken, A., Ercisli, S., Guleryuz, M., Donmez, M. F., and Sahin, F. (2006). Biological control of brown rot (Moniliana laxa Ehr.) on apricot (Prunus armeniaca L. cv. Hacihaliloglu) 

by Bacillus, Burkholdria, and Pseudomonas application under in vitro and in vivo conditions. Biological Control 38, 369-372. 

Bonaterra, A., Frances, J. M., Moreno, M. C., Badosa, E., and Montesinos, E. (2004). Post-harvest biological control of a wide range of fruit types and pathogens by Pantoea agglomerans EPS125. Bulletin 

OILB/SROP 27, 357-360. 

Bonaterra, A., Mari, M., Casalini, L., and Montesinos, E. (2003). Biological control of Monilinia laxa and Rhizopus stolonifer in postharvest of stone fruit by Pantoea agglomerans EPS125 and putative 

mechanisms of antagonism. International Journal of Food Microbiology 84, 93-104. 

Cal, A. d., Larena, I., Guijarro, B., and Melgarejo, P. (2002). Mass production of conidia of Penicillium frequentans, a biocontrol agent against brown rot of stone fruits. Biocontrol Science and Technology 12, 

715-725. 

Cal, A. d., Larena, I., Torres, R., Linan, M., Domenichini, P., Bellini, A., Mandrin, J. F., Ochoa de Eribe, X., Usall, J., and Melgarejo, P. (2004). Control of brown rot of peaches caused by Monilinia spp. by 

preharvest treatments. In "Recent research developments in plant pathology, Vol. 3", pp. 85-98. 

Cal, A. d., Sagasta, E. M., and Melgarejo, P. (1990). Biological control of peach twig blight (Monilinia laxa) with Penicillium frequentans. Plant Pathology 39, 612-618. 

Cardei, E. (2001). Trichodex and Silposan - long-term biological preparations in phytoprotection of sweet cherry tree and sour cherry tree. Cercetari Agronomice in Moldova 34, 119-122. 

Dedej, S., Delaplane, K. S., and Scherm, H. (2004). Effectiveness of honey bees in delivering the biocontrol agent Bacillus subtilis to blueberry flowers to suppress mummy berry disease. Biological Control 

31, 422-427. 

Droby, S., Wisniewski, M., El-Ghaouth, A., and Wilson, C. (2003). Influence of food additives on the control of postharvest rots of apple and peach and efficacy of the yeast-based biocontrol product Aspire. 


El-Sheikh Aly, M. M., Baraka, M. A., and El-Sayed Abbass, A. G. (2000). The effectiveness of fumigants and biological protection of peach against fruit rots. Assiut Journal of Agricultural Sciences 31, 19- 

31. 

Esitken, A., Ercisli, S., Karlidag, H., and Sahin, F. (2005). Potential use of plant growth promoting rhizobacteria (PGPR) in organic apricot production. In "Proceedings of the international scientific 

conference: Environmentally friendly fruit growing, Polli, Estonia, 7-9 September, 2005", pp. 90-97. 

Falconi, C. J., and Mendgen, K. (1994). Epiphytic fungi on apple leaves and their value for control of the postharvest pathogens Botrytis cinerea, Monilinia fructigena and Penicillium expansum. Zeitschrift fur 

Pflanzenkrankheiten und Pflanzenschutz 101, 38-47. 

Fan, Q., Tian, S., Jiang, A., and Xu, Y. (2001). Isolation and screening of biocontrol antagonists of diseases of postharvest fruits. China Environmental Science 21, 313-316. 

Foschi, S., Roberti, R., Brunelli, A., and Flori, P. (1995). Application of antagonistic fungi against Monilinia laxa agent of fruit rot of peach. Bulletin OILB/SROP 18, 79-82. 

Grebenisan, I., Cornea, C. P., Mateescu, R., Olteanu, V., and Voaides, C. (2006). Control of postharvest fruit rot in apricot and peach by Metschnikowia pulcherrima. Buletinul Universitatii de Stiinte Agricole 

si Medicina Veterinara Cluj-Napoca. Seria Agricultura 62, 74-79. 

Grebenisan, I., Cornea, P., Mateescu, R., Cimpeanu, C., Olteanu, V., Campenu, G., Stefan, L. A., Oancea, F., and Lupu, C. (2008). Metschnikowia pulcherrima, a new yeast with potential for biocontrol of 

postharvest fruit rots. Acta Horticulturae, 355-360. 

Gueldner, R. C., Reilly, C. C., Pusey, P. L., Costello, C. E., Arrendale, R. F., Cox, R. H., Himmelsbach, D. S., Crumley, F. G., and Cutler, H. G. (1988). Isolation and identification of iturins as antifungal 

peptides in biological control of peach brown rot with Bacillus subtilis. Journal of Agricultural and Food Chemistry 36, 366-370. 

125


Haseli, A., and Weibel, F. (2002). Disease control in organic cherry production with new products and early plastic cover of the trees. In "11th International Conference on Cultivation Technique and 

Phytopathological Problems in Organic Fruit-Growing. Proceedings of the conference, Weinsberg, Germany, 3-5 February 2004", pp. 122-130. 

Hong, C., Michailides, T. J., and Holtz, B. A. (1998). Effects of wounding, inoculum density, and biological control agents on postharvest brown rot of stone fruits. Plant Disease 82, 1210-1216. 

Karabulut, O. A., and Baykal, N. (2003). Biological control of postharvest diseases of peaches and nectarines by yeasts. Journal of Phytopathology 151, 130-134. 

Karabulut, O. A., Cohen, L., Wiess, B., Daus, A., Lurie, S., and Droby, S. (2002). Control of brown rot and blue mold of peach and nectarine by short hot water brushing and yeast antagonists. Postharvest 


Larena, I., Cal, A. d., and Melgarejo, P. (2001). Biological control of Monilinia laxa on stone fruits. Bulletin OILB/SROP 24, 313-317. 

Larena, I., and Melgarejo, P. (1996). Biological control of Monilinia laxa and Fusarium oxysporum f.sp. lycopersici by a lytic enzyme-producing Penicillium purpurogenum. Biological Control 6, 361-367. 

Larena, I., Torres, R., Cal, A. d., Linan, M., Melgarejo, P., Domenichini, P., Bellini, A., Mandrin, J. F., Lichou, J., Ochoa de Eribe, X., and Usall, J. (2005). Biological control of postharvest brown rot 

(Monilinia spp.) of peaches by field applications of Epicoccum nigrum. Biological Control 32, 305-310. 

Madrigal, C., Pascual, S., and Melgarejo, P. (1994). Biological control of peach twig blight (Monilinia laxa) with Epicoccum nigrum. Plant Pathology 43, 554-561. 

Mari, M., Torres, R., Casalini, L., Lamarca, N., Mandrin, J. F., Lichou, J., Larena, I., Cal, M. A. d., Melgarejo, P., and Usall, J. (2007). Control of post-harvest brown rot on nectarine by Epicoccum nigrum and 

physico-chemical treatments. Journal of the Science of Food and Agriculture 87, 1271-1277. 

McKeen, C. D., Reilly, C. C., and Pusey, P. L. (1986). Production and partial characterization of antifungal substances antagonistic to Monilinia fructicola from Bacillus subtilis. Phytopathology 76, 136-139. 

McLaughlin, R. J., Wilson, C. L., Droby, S., Ben-Arie, R., and Chalutz, E. (1992). Biological control of postharvest diseases of grape, peach, and apple with the yeasts Kloeckera apiculata and Candida 

guilliermondii. Plant Disease 76, 470-473. 

Melgarejo, P., Carrillo, R., and Sagasta, E. M. (1986). Potential for biological control of Monilinia laxa in peach twigs. Crop Protection 5, 422-426. 

Mercier, J., and Jimenez, J. I. (2004). Control of fungal decay of apples and peaches by the biofumigant fungus Muscodor albus. Postharvest Biology and Technology 31, 1-8. 

Migheli, Q., Gullino, M. L., Piano, S., Galliano, A., and Duverney, C. (1997). Biocontrol capability of Metschnikowia pulcherrima and Pseudomonas syringae against postharvest rots of apple under semicommercial 

condition. Mededelingen - Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, Universiteit Gent 62, 1065-1070. 

Ngugi, H. K., Dedej, S., Delaplane, K. S., Savelle, A. T., and Scherm, H. (2005). Effect of flower-applied Serenade biofungicide (Bacillus subtilis) on pollination-related variables in rabbiteye blueberry. 


Pascual, S., Melgarejo, P., and Naresh, M. (2000). Accumulation of compatible solutes in Penicillium frequentans grown at reduced water activity and biocontrol of Monilinia laxa. Biocontrol Science and 


Pusey, P. L. (1989). Use of Bacillus subtilis and related organisms as biofungicides. Pesticide Science 27, 133-140. 

Pusey, P. L., Hotchkiss, M. W., Dulmage, H. T., Baumgardner, R. A., Zehr, E. I., Reilly, C. C., and Wilson, C. L. (1988). Pilot tests for commercial production and application of Bacillus subtilis (B-3) for 

postharvest control of peach brown rot. Plant Disease 72, 622-626. 

Pusey, P. L., and Wilson, C. L. (1984). Postharvest biological control of stone fruit brown rot by Bacillus subtilis. Plant Disease 68, 753-756. 

Pusey, P. L., Wilson, C. L., Hotchkiss, M. W., and Franklin, J. D. (1986). Compatibility of Bacillus subtilis for postharvest control of peach brown rot with commercial fruit waxes, dicloran, and cold-storage 

conditions. Plant Disease 70, 587-590. 

Qin, G. Z., and Tian, S. P. (2005). Enhancement of biological control activity of Cryptococcus laurentii by silicon and the possible mechanisms involved. Phytopathology 95, 69-75. 

Qin, G. Z., Tian, S. P., Xu, Y., Chan, Z. L., and Li, B. Q. (2006). Combination of antagonistic yeasts with two food additives for control of brown rot caused by Monilinia fructicola on sweet cherry fruit. 

Journal of Applied Microbiology 100, 508-515. 

Ritte, E., Lurie, S., Droby, S., Ismailov, Z., Chet, I., and Chernin, L. (2002). Biocontrol of postharvest fungal pathogens of peaches and apples by Pantoae agglomerans strain IC1270. Bulletin OILB/SROP 25, 

199-202. 

Schena, L., Nigro, F., Pentimone, I., Ligorio, A., and Ippolito, A. (2003). Control of postharvest rots of sweet cherries and table grapes with endophytic isolates of Aureobasidium pullulans. Postharvest 


Scherm, H., Ngugi, H. K., Savelle, A. T., and Edwards, J. R. (2004). Biological control of infection of blueberry flowers caused by Monilinia vaccinii-corymbosi. Biological Control 29, 199-206. 

Scherm, H., and Stanaland, R. D. (2001). Evaluation of fungicide timing strategies for control of mummy berry disease of rabbiteye blueberry in Georgia. Small Fruits Review 1, 69-81. 

Schilder, A. M. C., Hancock, J. F., and Hanson, E. J. (2006). An integrated approach to disease control in blueberries in Michigan. Acta Horticulturae, 481-488. 

Schnabel, G., and Mercier, J. (2006). Use of a Muscodor albus pad delivery system for the management of brown rot of peach in shipping cartons. Postharvest Biology and Technology 42, 121-123. 

Shevchuk, I. V. (2006). Efficiency of biofungicides against dominating diseases of cherries and plums under the different climatic conditions of Ukraine. Phytopathologia Polonica, 125-131. 

126

Appendix 5 

Smilanick, J. L., Denis-Arrue, R., Bosch, J. R., Gonzalez, A. R., Henson, D., and Janisiewicz, W. J. (1993). Control of postharvest brown rot of nectarines and peaches by Pseudomonas species. Crop 

Protection 12, 513-520. 

Spadaro, D., Vola, R., Piano, S., and Gullino, M. L. (2002). Mechanisms of action and efficacy of four isolates of the yeast Metschnikowia pulcherrima active against postharvest pathogens on apples. 


Spotts, R. A., Cervantes, L. A., and Facteau, T. J. (2002). Integrated control of brown rot of sweet cherry fruit with a preharvest fungicide, a postharvest yeast, modified atmosphere packaging, and cold storage 

temperature. Postharvest Biology and Technology 24, 251-257. 

Stevens, C., Khan, V. A., Lu, J. Y., Wilson, C. L., Pusey, P. L., Igwegbe, E. C. K., Kabwe, K., Mafolo, Y., Liu, J., Chalutz, E., and Droby, S. (1997). Integration of ultraviolet (UV-C) light with yeast treatment 

for control of postharvest storage rots of fruits and vegetables. Biological Control 10, 98-103. 

Stevens, C., Khan, V. A., Lu, J. Y., Wilson, C. L., Pusey, P. L., Kabwe, M. K., Igwegbe, E. C. K., Chalutz, E., and Droby, S. (1998). The germicidal and hormetic effects of UV-C light on reducing brown rot 

disease and yeast microflora of peaches. Crop Protection 17, 75-84. 

Thornton, H. A., Savelle, A. T., and Scherm, H. (2008). Evaluating a diverse panel of biocontrol agents against infection of blueberry flowers by Monilinia vaccinii-corymbosi. Biocontrol Science and 


Tian, S., Qin, G., and Xu, Y. (2004). Survival of antagonistic yeasts under field conditions and their biocontrol ability against postharvest diseases of sweet cherry. Postharvest Biology and Technology 33, 

327-331. 

Utkhede, R. S., and Sholberg, P. L. (1986). In vitro inhibition of plant pathogens by Bacillus subtilis and Enterobacter aerogenes and in vivo control of two postharvest cherry diseases. Canadian Journal of 


Wang, Y., and Tian, S. (2007). Interaction between Cryptococcus laurentii, Monilinia fructicola and sweet cherry fruit at different temperatures. Scientia Agricultura Sinica 40, 2811-2820. 

Wisniewski, M., Wilson, C., El-Ghaouth, A., and Droby, S. (2001). Increasing the ability of the biocontrol product, Aspire, to control postharvest diseases of apple and peach with the use of additives. Bulletin 

OILB/SROP 24, 157-160. 

Wittig, H. P. P., Johnson, K. B., and Pscheidt, J. W. (1997). Effect of epiphytic fungi on brown rot blossom blight and latent infections in sweet cherry. Plant Disease 81, 383-387. 

Xu, X., Chan, Z., Xu, Y., and Tian, S. (2008). Effect of Pichia membranaefaciens combined with salicylic acid on controlling brown rot in peach fruit and the mechanisms involved. Journal of the Science of 

Food and Agriculture 88, 1786-1793. 

Yao, H. J., and Tian, S. P. (2005). Effects of a biocontrol agent and methyl jasmonate on postharvest diseases of peach fruit and the possible mechanisms involved. Journal of Applied Microbiology 98, 941- 

950. 

Zhou, T., Northover, J., and Schneider, K. E. (1999). Biological control of postharvest diseases of peach with phyllosphere isolates of Pseudomonas syringae. Canadian Journal of Plant Pathology 21, 375- 

381. 

Zhou, T., Schneider, K. E., and Li, X. (2008). Development of biocontrol agents from food microbial isolates for controlling post-harvest peach brown rot caused by Monilinia fructicola. International Journal 

of Food Microbiology 126, 180-185. 

127

Appendix 6. Primary literature (2007-2009) on biological control against Fusarium oxysporum 

Abo-Elyousr, K. A. M. and H. M. Mohamed (2009). "Biological Control of Fusarium Wilt in Tomato by Plant Growth-Promoting Yeasts and Rhizobacteria." Plant Pathology Journal 25(2): 199-204. 

Three plant growth-promoting yeasts and two rhizobacteria were tested for controlling tomato wilt caused by Fusarium oxysporum L sp. lycopersici under greenhouse and field conditions. Under 

greenhouse and field conditions, all treatments were significantly reduced disease severity of tomato wilt relative to the infected control. The highest disease reductions in pots (75.0, 67.4%) and field 

(52.5, 42.4%) were achieved by Azospirillum brasilense and Bacillus subtilis compared to infected control. Under field condition all treatments produced the highest tomato yield compared to the control 

plants inoculated with the pathogen 

. 

Al-Jedabi, A. A. (2009). "Biological control of Fusarium root-rot of sorghum." Research Journal of Agriculture and Biological Sciences 5(4): 465-473. 

several crops including sorghum that result in low grain yield. All antagonists showed inhibition of mycelial growth of F. oxysporum and the maximum inhibition was recorded when Bacillus subtilis as 

biocontrol agent (67.7%). The in vitro root colonization study demonstrated that after four days of germination, the cell counts obtained from the roots have increased and the maximum count is achieved 

by B. subtilis (16.9*105 cfu/cm root). The greenhouse pot experiment demonstrated that T. viride and B. subtilis resulted in more than 80% suppression of root rot. The reduction in fresh weight of roots 

amounted to 93.6% in the control treatment inoculated with F. oxysporum alone, whereas 71.1% reduction in fresh root weight was recorded for the treatments inoculated with both the pathogen and B. 

subtilis; 66.8% reduction in fresh root weight was recorded for the treatments inoculated with both the pathogen and T. harzianum. Root dry weight of the control treatment inoculated with only F. 

oxysporum decreased by 94.5% in relation to the non-inoculated control. Among the potential biological control agents in this study, B. cereus resulted in 42.3 reduction in root dry weight compared to 

the 94.5% reduction recorded for the control inoculated with F. oxysporum alone. 100% of the roots from the control treatment (F. oxysporum only) rendered growth of F. oxysporum compared to an 

incidence ranging from 20 to 55% for plants treated with B. subtilis, B. lecheniformis, B. cereus, T. harzianum and T. viride. Both chlorophyll fractions increased when treated with antagonist and the 

maximum enhancement was recorded when Bacillus subtilis used as antagonist compared with that of control. The maximum values of the carbohydrate components were recorded when Bacillus 

subtilis used as antagonist relative to those of control. 

Amini, J. (2009). "Induced Resistance in Tomato Plants Against Fusarium Wilt Invoked by Nonpathogenic Fusarium, Chitosan and Bion." Plant Pathology Journal 25(3): 256-262. 

The potential of nonpathogenic Fusarium oxysporum strain Avr5, either alone or in combination with chitosan and Bion, for inducing defense reaction in tomato plants inoculated with E oxyysporum f. 

sp lycopersici, was studied in vitro and glasshouse conditions. Application Bion at concentration of 5, 50, 100 and 500 mu g/ml, and the highest concentration of chitosan reduced in vitro growth of the 

pathogen. Nonpathogenic F oxysporum Avr5 reduced the disease severity of Fusarium wilt of tomato in split plants, significantly. Bion and chitosan applied on tomato seedlings at concentration 100 mu 

g a.i./plant; 15, 10 and 5 days before inoculation of pathogen. All treatments significantly reduced disease severity of Fusarium wilt of tomato relative to the infected control. The biggest disease reduction 

and increasing tomato growth belong to combination of nonpathogenic Fusarium and Bion. Growth rate of shoot and root markedly inhibited in tomato plants in response to tomato Fusarium wilt as 

compared with healthy control. These results suggest that reduction in disease incidence and promotion in growth parameters in tomato plants inoculated with nonpathogenic Fusarium and sprayed with 

elicitors could be related to the synergistic and cooperative effect between them, which lead to the induction and regulation of disease resistance. Combination of elicitors and nonpathogenic Fusarium 

synergistically inhibit the growth of pathogen and provide the first experimental support to the hypothesis that such synergy can contribute to enhanced fungal resistance in tomato. This chemical could 

provide a new approach for suppression of tomato Fusarium wilt, but its practical use needs further investigation. 

Anand, R., S. Kulothungan, et al. (2009). "Assay of chitinase and beta-1,3 glucanase in Gossypium hirsutum seedlings by Trichoderma spp. against Fusarium oxysporum." International Journal of Plant 

Sciences (Muzaffarnagar) 4(1): 255-258. 

wilt in cotton. In this regard, the six species of Trichoderma, namely T. viride, T. virens [Gliocladium virens], T. hamatum, T. harzianum, T. koningii and T. reesi, were evaluated for its biocontrol 

properties and induction of defence-related enzymes, namely chitinase and beta1-3-glucanase in 30 days old cotton (G. hirsutum) seedlings. Trichoderma spp. could efficiently control the growth rate of 

F. oxysporum. In vitro assay of chitinase and beta-1,3-glucanase revealed the maximum production by T. harzianum (56 U/ml) and T. hamatum (80 U/ml), respectively. It also produced appreciable 

quantities of defence enzymes. The maximum induction of chitinase and beta1-3-glucanase in plants was found to be 80 U/ml when challenged with T. harzianum, in addition to the enhancement of 

defence mechanism in plants. Trichoderma spp. improved the germination rate of seedlings. 

Anitha, A. and M. Rebeeth (2009). "Self-fusion of Streptomyces griseus enhances chitinase production and biocontrol activity against Fusarium oxysporum f. sp. lycopersici." Biosciences, Biotechnology 

Research Asia 6(1): 175-180. 

Protoplasts were isolated from Streptomyces griseus (MTCC - *4734) strain using lysing enzymes and self-fusion of Streptomyces griseus protoplasts was carried out using 50% polyethylene glycol 

(MW 1000, Sigma Chemicals Co., USA) in protoplast buffer. The regenerated 8 self fused Streptomyces griseus were studied detailed for chitinase production and biocontrol activity. Parent strain (PSg) 

128

Appendix 6 

showed protein content of 2.7 mg/ml with chitinase activity of 120 IU/ml. High chitinase activity was measured in the culture filtrates of most of the self-fusants (87%) than the parent. Among the 

fusants, the strain SFSg 5 produced protein content of 7.8 mg/ml, maximum chitinase activity of 283.3 IU/ml with a two-fold increase as compared to the parent strain. All the self-fusants exhibited 

increased antagonistic activity against F. oxysporum f. sp. lycopersici than the parent. Maximum inhibition (82%, 80%) of mycelial growth of F. oxysporum was recorded with fusant of SFSg 5, SFSg 1 

as against 61.1% with PSg. The result implies that, the self-fused Streptomyces griseus resulted in appreciable increase of chitinase production and biocontrol activity also the significance of the 

protoplast fusion technique, which could successfully be used to develop hybrid strains also for commercial formulation. 

Baysal, O., M. Calskan, et al. (2008). "An inhibitory effect of a new Bacillus subtilis strain (EU07) against Fusarium oxysporum f. sp. Radicis-lycopersici." PMPP Physiological and Molecular Plant 

Pathology 73(1/3): 25-32. 

destructive disease on tomato (Lycopersicon esculentum Mill.) transplant seedlings and the causal organism of crown and root rot of tomato plants growing in southern coast greenhouses of Turkey. An 

isolate of Bacillus subtilis (EU07) identified by the 16s RNA region code gene was selected as the best antagonist and evaluated against FORL in vitro studies. Strain EU07 at 106 CFU ml-1 was able to 

reduce disease incidence by 75%, when applied as an inoculant. It efficiently inhibited FORL compared to the control and QST 713 (AgraQuest, Davis, CA) whose inhibition ratio was only 52% in vivo. 

Random amplified polymorphic DNA analyses showed banding (genetic) differences between EU07 and QST 713 whereas there were no differences between DNAs of strains that have high homology 

to genes involved in the synthesis of antibiotics fengycin, bacillomycin and iturin when screened by oligonucleotide primers designed based on sequence information obtained from the NCBI database. 

Furthermore, one specific fragment in the EU07 genome showed the highest similarity to YrvN protein by 99% and AAA ATPase domain protein (72.2%) after amplifying oligonucleotide primers that 

are specific to the N-acyl-homoserine lactonase (HLS) gene as a biocontrol activity marker. These results suggested an effect of EU07 on control FORL by YrvN protein as subunit of protease enzyme. 

Furthermore, this fragment associated with HLS gene may be a potential molecular marker for selecting effective biological control agent belonging to Bacillus in order to control soilborne pathogens 

such as Fusarium, suggesting impairment in FORL invasion by signaling in the plant rhizosphere. 

Bernal-Vicente, A., M. Ros, et al. (2009). "Increased effectiveness of the Trichoderma harzianum isolate T-78 against Fusarium wilt on melon plants under nursery conditions." Journal of the Science of Food 

and Agriculture 89(5): 827-833. 

BACKGROUND: The use of isolates of the genus Trichoderma to control Fusarium wilt in melon plants is one of the most recent and effective alternatives to chemical treatments. In this work we have 

studied the immobilization of the isolate Trichoderma harzianum T-78 on different carriers as an efficient method to control vascular Fusarium wilt of melon in nurseries. Different formulations were 

developed: liquids (spore suspension, guar gum and carboxymethylcellulose) and solids (bentonite, vermiculite and wheat bran). RESULTS: The introduction of F. oxysporum resulted in a significant 

decrease in seedling fresh weight. The treatments which gave a lesser reduction in weight and showing a greater biocontrol effect were the liquid conidial suspension and the solid treatments with 

bentonite and superficial vermiculite. Microbiological analyses revealed that the conidial suspension and all the solid treatments, except wheat bran, significantly decreased F. oxysporum populations. Of 

all the treatments assayed, bentonite produced the greatest decline in the F. oxysporum population. CONCLUSIONS: The most effective treatments against Fusarium wilt on melon plants were the solid 

treatments bentonite and superficial vermiculite. These two treatments gave the greatest plant weight, the lowest percentage of infected plants and the greatest T. harzianum population throughout the 

assay. (C) 2009 Society of Chemical Industry 

Boureghda, H. and Z. Bouznad (2009). "Biological control of Fusarium wilt of chickpea using isolates of Trichoderma atroviride, T. harzianum and T. longibrachiatum." Acta Phytopathologica et 

Entomologica Hungarica 44(1): 25-38. 

The efficiency of the antagonist species Trichoderma atroviride (strains Ta.3, Ta.7 and Ta.13), T. harzianum (Th.6, Th.12, Th.15, Th.16 and Th.18) and T. longibrachiatum (TL.1, TL.2, TL.4, TL.5, TL.8, 

TL.9, TL.10, TL.11, TL.14 and TL17) against Fusarium wilt (caused by Fusarium oxysporum f.sp. ciceris) was compared using in vitro- and in vivo-based bioassay. A significant decrease of both 

growth and conidia production of the pathogen was obtained compared to the control. The highest percentages of diameter colony reduction and conidial production were obtained with Ta.13, causing 

65.64% reduction in colony diameter (direct confrontation), 48.71% reduction in colony diameter (indirect confrontation), and a complete inhibition of conidial production. Once more in direct 

confrontation, T. atroviride overgrowth the pathogen colony and sporulate above. The seed treatment by Trichoderma spp. isolates before sowing in a soil already infested by the pathogen led to a 

significant decrease of disease severity compared to the untreated control. The weakest index of disease severity was obtained with Ta.13, which caused 83.92% reduction compared to the control. The 

most effective isolates in protecting chickpea seedlings against the disease were Ta.3, Ta.7 and Ta.13 as well as Th.16. The reduction of disease severity was associated with an increase of the vegetal 

growth including the stem height as well as the plant fresh and dry weights. 

129


Casimiro Michel-Aceves, A., M. Antonio Otero-Sanchez, et al. (2009). "In vitro biocontrol of Fusarium subglutinans (Wollenweb. and Reinking) Nelson, Toussoun and Marasas and F. oxysporum Schlecht., 

causal agents of "Witches' broom" of mango (Mangifera indica L.) by Trichoderma spp." Revista Mexicana de Fitopatologia 27(1): 18-26. 

The antagonistic effect of native strains of Trichoderma spp. was evaluated in vitro against Fusarium oxysporum (Fo) and Fusarium subglutinans (Fs), causal agents of mango "witches' broom". Ten 

strains of the antagonistic fungus were isolated, one of which was selected and identified to the species level (T. harzianum); this species showed the highest percentage of antagonism inhibiting mycelial 

growth of Fo by 62.9% and 42.0% of Fs. In dual Cultures between Fo and/or Fs with the selected strains of Trichoderma, the time for the first contact for Fo was between 3 and 4 days, and between 2 and 

3 for Fs. The greatest intersection area (0.87 cm) was observed in T. lignorum against Fo, while the intersection area in Fs with the native strain Thzn-2 was 0.85 cm. Native strains Thzn-2 and Thzcf-12, 

and the commercial one showed antagonism class 2, being able to stop growth of both plant pathogens. Strain Thzn-2 is promising as an alternative for biocontrol of Fo and Fs; however, it is necessary to 

evaluate it under field conditions. 

Chebotar, V. K., N. M. Makarova, et al. (2009). "Antifungal and phytostimulating characteristics of Bacillus subtilis Ch-13 rhizospheric strain, producer of bioprepations." Applied Biochemistry and 

Microbiology 45(4): 419-423. 

Bacillus subtilis Ch-13 industrial strain was shown to have a wide spectrum of antagonistic activities against different species of phytopathogenic fungi and bacteria. The B. subtilis Ch-13 strain produces 

lytic enzymes; cyanide and other antifungal metabolites; stimulates plant growth, producing phytohormones-auxin derivatives. This strain by 2.5 times reduced the quantity of tomato plants infected with 

phytopathogenic fungus Fusarium oxysporum during inoculation. Fungi abundance on roots with bacterial inoculation was 6.9 times less than in the absence of inoculation. The application of detected 

antifungal metabolites as biochemical markers for the strain enables to control the stability of physiologic and biochemical characteristics of the producer, and ensures a rapid quality assay of 

biopreparations with high performance liquid chromatography (HPLC). 

Chen, L. and W. Chen (2009). "Genome shuffling enhanced antagonistic activity against Fusarium oxysporum f. sp. melonis and tolerance to chemical fungicides in Bacillus subtilis BS14." Journal of Food, 

Agriculture & Environment 7(2): 856-860. 

enhance antagonistic activity against Fusarium oxysporum f. sp. melonis (FOM) and tolerance to two chemical fungicides. Strain BS14 was identified as a strain of Bacillus subtilis by the analysis of 16S 

rDNA sequences. A stable recombinant F35 was obtained after three rounds of shuffling. Antagonistic activity of recombinant F35 against FOM was increased by 34.52% and 65.48% compared to that 

of the parent strain HN8-7 with highest activity and another parent strain utilized, BS14. The tolerance to chemical fungicides was also significantly improved (p0.05) compared to that of strain BS14. 

Reduction of FOM of 94% was observed by using recombinant F35, which was increased by 45% compared to that of strain BS14 (p0.05) and no significant differences (p>0.05) compared to that of 

thiophanate methyl (MRL). Reduction of FOM of 100% was dramatically observed by using an integrated treatment combining MRL (50% of usual dosage) with recombinant F35. Strain F35 with these 

improved traits would be a promising biocontrol agent in the control of FOM. Here genome shuffling was proved to be a practical methodology for strain improvement of antagonistic microorganism 

Bacillus subtilis BS14 for enhancing antagonistic activity against FOM and tolerance to chemical fungicides. 

Clematis, F., M. L. Gullino, et al. (2009). "Antagonistic activity of microorganisms isolated from recycled soilless substrates against Fusarium crow rot." Protezione delle Colture(3): 29-33. 

We report the results obtained in biological control trials against crown and root rot of tomato incited by Fusarium oxysporum f. sp. radicis lycopersici by using microorganisms isolated from soilless 

cultivation systems that showed suppressiveness against this disease. Among the tested microorganisms belonging to fluorescent bacteria (32 isolates) and to fungi belonging to Trichoderma (39 isolates) 

and Fusarium (38 isolated), 5 bacteria and 6 fungi showed a good activity against the pathogen. Such strains will be used in greenhouse trials, under situations closer to the field, in order to evaluate their 

potential to be adopted under practical conditions. 

Eden Paredes-Escalante, J., J. Armando Carrillo-Fasio, et al. (2009). "Antagonistic microorganismos for control of the fungal complex that cause wilt in chickpea (Cicer arietinum L.) in the state of Sinaloa, 

Mexico." Revista Mexicana de Fitopatologia 27(1): 27-35. 

The antagonistic activity in vitro of microorganisms isolated from chickpea rhizosphere, was evaluated against Fusarium oxysporum, Sclerotium rolfsii, and Rhizoctonia solani, causal agents of chickpea 

wilt. The native strains with the higher percentage of pathogen mycelial growth inhibition were selected and identified as Trichoderma lignorum (CIAD 06-540903), T. harzianum (CIAD 05-550903), 

Bacillus subtilis (CIAD-940111), and Pseudomonas fluorescens (CIAD-990111). These strains and a commercial strain of T. harzianum (T-22) were mixed with Glomus intraradices and their 

effectiveness to reduce chickpea wilt was compared against a chemical treatment (PCNB) and all absolute control in the field. The seed was treated with the microorganisms before sowing and 

evaluations of disease severity were conducted each 15 days, while root colonization by the antagonistic microorganisms was assessed 45 days after sowing. Colonization of T, harzianum CIAD 05- 

550903 + G. infraradices was 33 x 10(3) ufc/g fresh root-75% and B. subtilis + G. intraradices was 1.3 x 10(8) Ufc/g fresh root-75%; while the combination P.fluorescens + G. intraradices was 1.4 x 

10(7) Ufc/g fresh root-88%. These treatments also showed a reduction of disease severity in 64, 57, and 51%, respectively in comparison with the control. 

130

Appendix 6 

El-Khallal, S. M. (2007). "Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors (jasmonic acid & salicylic 

acid): 2 - changes in the antioxidant enzymes, phenolic compounds and pathogen related-proteins." Australian Journal of Basic and Applied Sciences 1(4): 717-732. 

Induction of plant defense against pathogen attack is regulated by a complex network of different signals. In the present study interaction between hormonal signals [jasmonic acid (JA) or salicylic acid 

(SA)] and bioagent [arbuscular mychorrhiza (AM) fungi] was used as new strategy to enhance tomato defense responses against wilt disease caused by Fusarium oxysporum (Fo). Thus changes in 

various physiological defenses including antioxidant enzymes, phenolic compounds and pathogenesis related (PR) proteins were investigated in leaves of tomato plants. Results appeared that production 

of reactive oxygen species (ROS), mainly H2O2 and O2 increasing the time of infection. Application with bioagent AM fungi and/or hormonal elicitors (JA & SA) markedly decreased these levels, 

while LOX activity greatly increased as compared with infected control. SA - treated plants had the highest MDA level but JA+AM fungi treated plants recorded the highest LOX activity. Infection by 

Fusarium oxysporm significantly increased activity of antioxidant enzymes (SOD, APX and CAT) in tomato leaves at different stages of growth. The highest activity was recorded in leaves of AM 

fungi+JA-treated plants, while treatments with SA especially when applied alone markedly decreased H2O2 scavenging enzymes (APX and CAT) and greatly increased SOD activity. Thus, imbalance 

between H2O2 - generation and scavenging enzymes in leaves may reflect a defense mechanism in tomato or a pathogenicity strategy of the fungus. Levels of certain phenolic acids greatly changed in 

tomato leaves in response to Fusarium oxysporum, AM fungi and hormonal elicitors. Benzoic and Galleic acids contents markedly decreased, however, contents of coumaric, cinnamic, chlorogenic and 

ferulic acids increased in leaves of all treatments. Also, activity of lignification enzymes POX, PPX and PAL significantly increased in leaves of infected tomato plants. JA-treated plants caused the 

highest POX and PPX activities, while SA-treated plants having the highest PAL activities. High accumulation of phenolic compounds and activity POX, PPX and PAL in these plants may reflect a 

component of many defense signals activated by bioagent and hormonal inducers which leading to the activation of power defense system in tomato against attack. Analysis of protein electrophoresis 

revealed that interaction between hormone signal (JA & SA) and bioagent AM fungi mediating the expression of the majority of different PR-proteins leading to increasing defense mechanism against 

Fusarium oxysporum infection. Thus, induction of protein bands of molecular weights 35, 33, 32, 31 (PR-2, beta-1, 3 glucanase), 30.5 and 27 (PR-3,-4, chitinase) in infected leaves indicated the 

important role which played in disease resistance. Finally, the new mechanism of the combination strategy between bioagent and hormonal signals (either synergistically or antagonistically) played 

important roles for increasing various defense systems and altering expression of defense genes which leading to different PR-proteins working together to increased resistance in tomato plants against 

wilt disease caused by Fusarium oxysporum. In addition, results revealed that defense mechanism in plants treated with AM fungi and JA are more effective than AM fungi plus SA-treated plants. 

Floch, G. l., J. Vallance, et al. (2009). "Combining the oomycete Pythium oligandrum with two other antagonistic fungi: root relationships and tomato grey mold biocontrol." Biological Control 50(3): 288- 

298. 

To reduce Pythium oligandrum biocontrol variability and improve its efficacy, experiments were performed by combining the oomycete with two other antagonistic fungi, Fusarium dishes, Fo47 or T. 

harzianum hyphae destroyed P. oligandrum cells by antibiosis and mycoparasitism processes; in the rhizosphere of tomato plants (Lycopersicon esculentum), the same antagonistic features were 

observed. However, in the rhizosphere, hyphae are frequently separated by a certain distance; this allows the coexistence and the persistence of the three microorganisms on the root systems. When 

introduced in the rhizosphere, Fo47 and P. oligandrum were able to penetrate the root tissues with Fo47 limited to the epidermal and upper layers of cortical cells while P. oligandrum colonized deeper 

tissue at a faster rate. The two antagonists were killed in few days within roots following elicited plant-defense reactions. T. harzianum was not able to penetrate root tissues. Root colonization with either 

P.oligandrum alone or in combination with Fo47 and/or T. harzianum resulted in systemic plant resistance which provided plant protection against Botrytis cinerea infection of leaves. The level of control 

and the expression of pathogenesis-related proteins (PR-proteins) in leaves were similar whatever the antagonistic microbial treatment applied to roots. 

Gay, M. I. T., Anonymous, et al. (2009). Substrates containing a Trichoderma asperellum strain for biological control of Fusarium and Rhizoctonia, Universidad de Barcelona. 

The strain of Trichoderma asperellum T34(2) CECT No. 20417 is useful for preparing substrates for biological control of vascular fusariose and death of plants caused by Rhizoctonia solani. The 

substrates can be peats, composts (hardwood compost, pine bark compost, cork compost, sludge compost from sewage treatment plants, garden residues, etc.) or formulations based on CPV-type 

compost (compost+peat+vermiculite). The fact that the substrates suppress both Fusarium oxysporum f. sp. lycopersici and Rhizoctonia solani provides an advantage in comparison with other substrates 

known in prior art. Another advantage is that the use of methyl bromide, a highly harmful product for the environment, in the control of vascular fusariose is avoided. 

Huang, X., J. Luo, et al. (2009). "Isolation and bioactivity of endophytic fungi in Derris hancei." Journal of South China Agricultural University 30(2): 44-47. 

Derris hancei Hemsl. The antagonism of endophytic fungi against fungal pathogens was tested in vitro. Penicillium sp. Q1, Rhizoctonia sp. S1, Phomopsis sp. N2, and Corticium sp. F1 isolated from the 

caudex of D. hancei, and Penicillium sp. Q2 isolated from the leaf, inhibited the hyphal growth of Colletotrichum gloeosporioides Penz, Fusarium oxysporum f. niveum (E. F. Smith) Snyber et Hansen, 

Rhizoctonia sp. S1 against Colletotrichum orbiculare Arx, and Phomopsis sp. N2 against Colletotrichum musae (Berk1 & Curt1) Arx1 on dual culture with inhibition index II. It was reported that 

endophytic fungus in D.hancei could produced antibacterial substances in this paper. The culture filtrates of Penicillium sp. Q2 treated in 48 h after treatment possessed 100.00% of adjusted mortality 

against the 2nd larvae of Spodoptera litura by leaves disc feeding bioassays, and 75.10% against Lipaphis erysimi Kaltenbach (apterous adult) by insect-soaking method, respectively, which showed that 

the activity of Penicillium sp. Q2 was higher than that of other endophytic fungi. 

131


Jadeja, K. B. and D. M. Nandoliya (2008). "Integrated management of wilt of cumin (Cuminum cyminum L.)." Journal of Spices and Aromatic Crops 17(3): 223-229. 

Four components of integrated management namely, soil solarization, crop rotation, chemicals and biocontrol agents were tested under field condition at Junagadh (Gujarat) for the management of wilt of 

cumin (Cuminum cyminum) caused by Fusarium oxysporum f. sp. cumini. Growing of sorghum (Sorghum bicolor) or maize (Zea mays) during kharif season did not reduce wilt incidence during the 

following rabi season. Soil solarization with 25 m LLDPE plastic cover for 15 days in summer proved most effective in reducing wilt incidence to 26.27% as against 44.90% in non-solarization and 

increasing yield to 396 kg ha-1 as against 286 kg ha-1 in non-solarized plots. Application of carbendazim granules @ 10 kg ha-1 one month after sowing or Trichoderma viride in organic carrier @ 62.5 

kg ha-1 at sowing time were also effective. Integrating soil solarization followed by growing of sorghum in kharif and application of either carbendazim granules @ 10 kg ha-1 one month after sowing or 

application of T.viride in organic carrier @ 62.5 kg ha-1 was effective for the management of cumin wilt. 

Kamilova, F., S. Validov, et al. (2009). Biological control of tomato foot and root rot caused by Fusarium oxysporum f.sp. radicis-lycopersici by Pseudomonas bacteria. Proceedings of the Second 

International Symposium on Tomato Diseases, Kusadasi, Turkey, 8-12 October 2007. 

Rhizobacteria are a natural and most suitable source for the isolation of potential microbiological control agents that can protect plants from soilborne pathogens and consequently improve crop quality 

and yield. The beneficial effect of such bacteria on plant health depends in many cases on their ability to aggressively colonize the rhizosphere and compete with the indigenous, including pathogenic, 

microflora for nutrients and niches on the plant root. Bacterial strains Pseudomonas chlororaphis PCL1391 and P. fluorescens WCS365 employ antibiosis and induced systemic resistance, respectively, to 

control tomato foot and root rot (TFRR) caused by phytopathogenic fungus Fusarium oxysporum f.sp. radicis-lycopersici (Forl). For the selection of biocontrol bacteria acting via the mechanism 

"competition for nutrients and niches" we have developed an enrichment method for enhanced tomato root tip colonizers, starting from a crude mixture of rhizobacteria coated on the seed, using a sterile 

quartz sand/plant nutrient solution gnotobiotic system. As a result of this enrichment procedure, and subsequent tests on competitive tomato root tip colonization, the strongly competitive biocontrol 

strains P. fluorescens PCL1751 and P. putida PCL1760 were isolated. Both strains effectively suppress TFRR under soil and hydroponic cultivation conditions. 

Kamilova, F., S. Validov, et al. (2009). "Biological control of tomato foot and root rot caused by Fusarium oxysporum f.sp. radicis-lycopersici by Pseudomonas bacteria." Acta Horticulturae(808): 317-320. 

isolation of potential microbiological control agents that can protect plants from soilborne pathogens and consequently improve crop quality and yield. The beneficial effect of such bacteria on plant 

health depends in many cases on their ability to aggressively colonize the rhizosphere and compete with the indigenous, including pathogenic, microflora for nutrients and niches on the plant root. 

Bacterial strains Pseudomonas chlororaphis PCL1391 and P. fluorescens WCS365 employ antibiosis and induced systemic resistance, respectively, to control tomato foot and root rot (TFRR) caused by 

phytopathogenic fungus Fusarium oxysporum f.sp. radicis-lycopersici (Forl). For the selection of biocontrol bacteria acting via the mechanism "competition for nutrients and niches" we have developed 

an enrichment method for enhanced tomato root tip colonizers, starting from a crude mixture of rhizobacteria coated on the seed, using a sterile quartz sand/plant nutrient solution gnotobiotic system. As a 

result of this enrichment procedure, and subsequent tests on competitive tomato root tip colonization, the strongly competitive biocontrol strains P. fluorescens PCL1751 and P. putida PCL1760 were 

isolated. Both strains effectively suppress TFRR under soil and hydroponic cultivation conditions. 

Kannan, V. and R. Sureendar (2009). "Synergistic effect of beneficial rhizosphere microflora in biocontrol and plant growth promotion." Journal of Basic Microbiology 49(2): 158-164. 

Biological systems are getting more relevance than chemical control of plant pathogens as they are not only eco-friendly and economic in approach but are also involved in improving the soil consistency 

and maintenance of natural soil flora. Plant growth promoting rhizosphere microorganisms were isolated from three different tree rhizospheres using selective culture media. Five microorganisms were 

selected from each rhizosphere soil based on their efficiency and screened for their ability to promote plant growth as a consortium. Each of the developed consortium has a phosphate solubilizer, 

nitrogen fixer, growth hormone producer, heterotrophic member and an antagonist. The plant growth promoting ability of the microbial members present in the consortium was observed by estimating 

the IAA production level and also by the nitrogenase activity of the nitrogen fixers. The biocontrol potentiality of the consortium and the antagonist present in the consortium were checked by both dual 

plate assay and cross-streaking technique. Consortial treatments effected very good growth promotion in Lycopersicon esculentum Mill and the treated plants also developed resistance against wilt 

pathogen, Fusarium oxysporum f. sp. lycopersici though the effect was well pronounced with consortium developed from Santalum album. 

Li, J., Q. Yang, et al. (2009). "Evaluation of biocontrol efficiency and security of A Bacillus subtilis strain B29 against cucumber Fusarium wilt in field." China Vegetables(2): 30-33. 

cucumerinum, was isolated from cucumber rhizosphere. After twice of 4-field-plot experiments, the control efficiencies of 100, 250 and 500 dilution times to cucumber Fusarium wilt were 70.3-88.2%, 

62.3-85.9%, and 54.7-80.6%, respectively. The average efficiency of field trials with B29 was 84.9% during 2 years and the yield of cucumber increased by 12.57%. The acute toxicity of Bacillus subtilis 

strain B29 to big mouse through its mouth and skin was examined, and the LD50 was more than 5000 mg/kg. The application of strain B29 on cucumber, tomato, bean and seed pumpkin was safe based 

on the observed seedling rate, growth and development. 

132

Appendix 6 

Liu, Q., J. C. Yu, et al. (2009). "Antagonism and Action Mechanism of Antifungal Metabolites from Streptomyces rimosus MY02." Journal of Phytopathology 157(5): 306-310. 

The genus of Streptomyces, a saprophytic Gram-positive bacterium, has properties, which make them useful as pharmaceutical and biocontrol agents. A streptomyces strain MY02 from soil samples 

showed significant antagonism against 14 plant pathogenic fungi including Fusarium oxysporum f. sp. cucumarinum. Antifungal metabolite(s) SN06 from the culture of the strain MY02 were extracted 

with n-butanol and purified by silica gel column chromatography. The minimum concentration of SN06 inhibiting any visible fungal growth of F. oxysporum f. sp. cucumarinum is 12.5 mu g/ml by 

twofold serial dilutions method. The mycelia of F. oxysporum f. sp. cucumarinum treated with SN06 were observed under the normal optics microscope. The results showed that some cells of hyphae 

began to dilate and formed some strings of beads. The cytoplasm oozed out of the cells with the culture time and so most of the cells became empty. The hyphae broke into many segments and then 

collapsed after 48 h. After inoculated in potato dextrose medium for 48 h, the filtrate of mycelia treated with 1% NaCl containing 12.5 mu g/ml SN06 was scanned using ultraviolet spectrophotometer 

and absorption peak at 260 nm showed that the mycelia cell membrane of F. oxysporum f. sp. cucumarinum was broken and that nucleic acid oozed out of the cell. 

Maina, M., R. Hauschild, et al. (2008). "Protection of tomato plants against fusaric acid by resistance induction." Journal of Applied Biosciences(JABs) 1: 18-31. 

Objectives: The rhizobacteria Bacillus sphaericus B43, Pseudomonas fluorescens T58, and P. putida 53 are able to induce systemic resistance (ISR) against Fusarium oxysporum f.sp. lycopersici (FOL) 

in tomato. This study investigated if the ISR reduced the damage by the toxin fusaric acid (FA) produced by FOL. Methodology and Results: The bacteria were applied to the rhizosphere of tomato 

plants. Chlorophyll content and ion leakage were determined after placing the leaf discs in FA. Active oxygen species (AOS), superoxide and hydrogen peroxide levels were determined in leaves of 

plants injected with FA. Activities of superoxide dismutase (SOD), ascorbate (AS) and guaiacol peroxidases (GPX) involved in AOS metabolism were quantified. In untreated plants, FA led to high ion 

leakage and chlorophyll degradation caused by H2O2 accumulation. All the bacteria treatments decreased the chlorophyll degradation. Ion leakage was reduced by treatment with P. fluorescens T58 and 

B. sphaericus B43, while P. putida 53 was less effective. Treatment of plants with bacteria resulted in increased superoxide contents, but varying over time. Increased SOD and GPX activities in untreated 

plants were suppressed after bacteria treatment. Plants treated with P. fluorescens T58 showed only a transient increase in superoxide. P. putida 53-treated plants removed AOS, but high initial superoxide 

levels led to membrane damages. Treatment with B. sphaericus B43 suppressed the effects of FA, but AOS metabolism showed only slight alterations. Conclusions and potential applications of findings: 

ISR could also protect plant tissues from damage by pathogen toxins, which is a potential new dimension to the known mechanisms of action of biological control agents. 

Martinez-Medina, A., J. A. Pascual, et al. (2009). "Interactions between arbuscular mycorrhizal fungi and Trichoderma harzianum and their effects on Fusarium wilt in melon plants grown in seedling 

nurseries." Journal of the Science of Food and Agriculture 89(11): 1843-1850. 

BACKGROUND: Biological control through the use of Trichoderma spp. and arbuscular mycorrhizal fungi (AMF) could contribute to a reduction of the inputs of environmentally damaging 

agrochemical products. The objective of this study was to evaluate the interactions between four AMF (Glomus intraradices, Glomus mosseae, Glomus claroideum and Glomus constrictum) and 

Trichoderma harzianum for their effects on melon plant growth and biocontrol of Fusarium wilt in seedling nurseries. RESULTS: AMF colonisation decreased fresh plant weight, which was unaffected 

by the presence of T. harzianum. Dual inoculation resulted in a decrease in fresh weight compared with AMF-inoculated plants, except for G. intraradices. AMF colonisation level varied with the AM 

endophyte and was increased by T. harzianum, except in G. mosseae-inoculated plants. Negative effects of AMF on T. harzianum colony-forming units were found, except with G. intraradices. AMF 

alone were less effective than T. harzianum in suppressing disease development. Combined inoculation resulted in a general synergistic effect on disease control. CONCLUSION: Selection of the 

appropriate AMF species and its combination with T. harzioanum were significant both in the formation and effectiveness of AM symbiosis and the reduction of Fusarium wilt incidence in melon plants. 

The combination of G. intraradices and T. harzianum provided better results than any other tested. (C) 2009 Society of Chemical Industry 

Matar, S. M., S. A. El-Kazzaz, et al. (2009). "Antagonistic and inhibitory effect of Bacillus subtilis against certain plant pathogenic fungi, I." Biotechnology 8(1): 53-61. 

subtilis isolates (B1 to B14), obtained from different Egyptian sites, were tested against six fungal isolates belonging to four different genera, Rhizoctonia solani, Helminthosporium spp., Alternaria spp. 

and Fusarium oxysporum. Cultural, morphological and physiological characteristics of these isolates were found to be identical to B. subtilis. Four B. subtilis isolates (B1, B4, B7, B8) had more 

antagonistic effect on all fungal isolates. Supernatant of B. subtilis isolate B7 had antagonistic effect on 6 fungal isolates but it was more effective on Helminthosporium spp., Alternaria spp. and F. 

oxysporum. B. subtilis as well as isolate B7 showed effectiveness in reducing disease incidence and severity levels of tomato plants when added to the F. oxysporum and R. solani-infested soil. Also, it 

stimulated the growth of tomato plants compared to the other. HPLC analysis of the HCl precipitate of B.subtilis isolate B7 culture supernatant revealed that an identical pattern of five peaks to that of a 

purified preparation of iturin A was obtained. 

Matar, S. M., S. A. El-Kazzaz, et al. (2009). "Bioprocessing and scaling-up cultivation of Bacillus subtilis as a potential antagonist to certain plant pathogenic fungi, III." Biotechnology 8(1): 138-143. 

isolate G-GANA7 (GenBank accession No. EF583053), collected from Abo-Homos in Egypt, was tested against six fungal isolates belonging to four different genera, i.e. Rhizoctonia solani, 

Helminthosporium sp., Alternaria sp. and Fusarium oxysporum. B. subtilis isolate G-GANA7 was cultured in 3 litre bench-top New Brunswick Scientific BioFlow III bioreactor for producing the 

maximum yield of biomass and antifungal compound. Fed-batch processes were automated through a computer aided data bioprocessing system AFS-BioCommand multi-process management program 

133


to regulate the cell growth rate by controlling interactively the nutrient feed rate, temperature, pH and agitation speed based on dissolved oxygen. In batch cultivation, the process suffered from low yield 

of cell mass (3.2 g litre-1) and antifungal activity because of high initial glucose concentration followed by acetate formation which the causal agent for inhibition of cell growth. Constant and exponential 

fed-batch strategies were adopted to circumvent this potential problem. Fed-batch cultivation of B. subtilis was conducted at the specific growth rate of 0.13 and 0.1 h-1 for constant and exponential 

strategies, respectively. High cell density of 12.8 and 14.6 g litre-1 for both operations, with an overall biomass yield of 0.45 g g-1 was achieved. The inhibitory activity of antifungal in supernatant 

reached its maximum value of 2 and 2.2 cm for constant and exponential fed-batch cultivations. 

Mazurier, S., T. Corberand, et al. (2009). "Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt." ISME Journal 3(8): 977-991. 

Natural disease-suppressive soils provide an untapped resource for the discovery of novel beneficial microorganisms and traits. For most suppressive soils, however, the consortia of microorganisms and 

mechanisms involved in pathogen control are unknown. To date, soil suppressiveness to Fusarium wilt disease has been ascribed to carbon and iron competition between pathogenic Fusarium oxysporum 

and resident non-pathogenic F. oxysporum and fluorescent pseudomonads. In this study, the role of bacterial antibiosis in Fusarium wilt suppressiveness was assessed by comparing the densities, 

diversity and activity of fluorescent Pseudomonas species producing 2,4-diacetylphloroglucinol (DAPG) (phlD+) or phenazine (phzC+) antibiotics. The frequencies of phlD+ populations were similar in 

the suppressive and conducive soils but their genotypic diversity differed significantly. However, phlD genotypes from the two soils were equally effective in suppressing Fusarium wilt, either alone or in 

combination with non-pathogenic F. oxysporum strain Fo47. A mutant deficient in DAPG production provided a similar level of control as its parental strain, suggesting that this antibiotic does not play a 

major role. In contrast, phzC+ pseudomonads were only detected in the suppressive soil. Representative phzC+ isolates of five distinct genotypes did not suppress Fusarium wilt on their own, but acted 

synergistically in combination with strain Fo47. This increased level of disease suppression was ascribed to phenazine production as the phenazine-deficient mutant was not effective. These results 

suggest, for the first time, that redox-active phenazines produced by fluorescent pseudomonads contribute to the natural soil suppressiveness to Fusarium wilt disease and may act in synergy with carbon 

competition by resident non-pathogenic F. oxysporum. 

Minerdi, D., S. Bossi, et al. (2009). "Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35." Environmental Microbiology 

11(4): 844-854. 

Fusarium oxysporum MSA 35 [wild-type (WT) strain] is an antagonistic Fusarium that lives in association with a consortium of bacteria belonging to the genera Serratia, Achromobacter, Bacillus and 

Stenotrophomonas in an Italian soil suppressive to Fusarium wilt. Typing experiments and virulence tests provided evidence that the F. oxysporum isolate when cured of the bacterial symbionts [the 

cured (CU) form], is pathogenic, causing wilt symptoms identical to those caused by F. oxysporum f. sp. lactucae. Here, we demonstrate that small volatile organic compounds (VOCs) emitted from the 

WT strain negatively influence the mycelial growth of different formae speciales of F. oxysporum. Furthermore, these VOCs repress gene expression of two putative virulence genes in F. oxysporum 

lactucae strain Fuslat10, a fungus against which the WT strain MSA 35 has antagonistic activity. The VOC profile of the WT and CU fungus shows different compositions. Sesquiterpenes, mainly 

caryophyllene, were present in the headspace only of WT MSA 35. No sesquiterpenes were found in the volatiles of ectosymbiotic Serratia sp. strain DM1 and Achromobacter sp. strain MM1. Bacterial 

volatiles had no effects on the growth of the different ff. spp. of F. oxysporum examined. Hyphae grown with VOC from WT F. oxysporum f. sp. lactucae strain MSA 35 were hydrophobic whereas 

those grown without VOCs were not, suggesting a correlation between the presence of volatiles in the atmosphere and the phenotype of the mycelium. This is the first report of VOC production by 

antagonistic F. oxysporum MSA 35 and their effects on pathogenic F. oxysporum. The results obtained in this work led us to propose a new potential direct long-distance mechanism for antagonism by F. 

oxysporum MSA 35 mediated by VOCs. Antagonism could be the consequence of both reduction of pathogen mycelial growth and inhibition of pathogen virulence gene expression. 

Nam, M. H., M. S. Park, et al. (2009). "Biological Control of Strawberry Fusarium Wilt Caused by Fusarium oxysporum f. sp fragariae Using Bacillus velezensis BS87 and RK1 Formulation." Journal of 

Microbiology and Biotechnology 19(5): 520-524. 

Two isolates, Bacillus sp. BS87 and RK1, selected from soil in strawberry fields in Korea, showed high levels of antagonism towards Fusarium oxysporum f. sp. fragariae in vitro. The isolates were 

identified as B. velezensis based on the homology of their gyrA sequences to reference strains. BS87 and RK1 were evaluated for control of Fusarium wilt in strawberries in pot trials and field trials 

conducted in Nonsan, Korea. In the pot trials, the optimum applied concentration of BS87 and RK1 for pre-plant root-dip application to control Fusarium wilt was 10(5) and 10(6) colony-forming units 

(CFU)/ml, respectively. Meanwhile, in the 2003 and 2005 field trials, the biological control efficacies of formulations of RK1 were similar to that of a conventional fungicide (copper hydroxide) when 

compared with a non-treated control. The RK1 formulation was also more effective than BS87 in suppressing Fusarium wilt under field conditions. Therefore, the results indicated that formulations of B. 

velezensis BS87 and RK1 may have potential to control Fusarium wilt in strawberries. 

Narayan, M., P. Tini, et al. (2009). "Biological and chemical management of tomato wilt caused by Fusarium oxysporum f.sp. lycopersici." Journal of Soils and Crops 19(1): 118-121. 

Wilt of tomato is one of the most important known disease caused by Fusarium oxysporum f. sp. lycopersici. In the present study four bioagents (Trichoderma harzianum, T. viride, Bacillus subtilis and 

Pseudomonas fluorescens) and two fungicides (Carbendazim and Thiram) were evaluated both in vitro and in vivo conditions. In vitro evaluation, of Carbendazim (0.1%) completely inhibited the growth 

134

Appendix 6 

of tomato wilt pathogen Fusarium oxysporum f.sp. lycopersici and was found significantly superior over the rest of fungicides. While, among the biological agents Trichoderma viride was found 

significantly superior to the rest in checking the growth of pathogens and showed 85.69 per cent inhibition. In vivo under field condition, seedling dip treatment of Carbendazim (1 gl-1 water) was found 

most significant followed by Carbendazim+ T.viride (1+100 gl-1 water) and T. viride (100 gl-1 water) significantly reduced wilt incidence by 73.91, 69.56 and 68.11 per cent respectively as against 

71.88 per cent wilting in control (under epiphytotic condition i.e. wilt sick soil). 

Ortega-Morales, B. O., F. N. Ortega-Morales, et al. (2009). "Antagonism of Bacillus spp. Isolated from Marine Biofilms Against Terrestrial Phytopathogenic Fungi." Marine Biotechnology 11(3): 375-383. 

We aimed at determining the antagonistic behavior of bacteria derived from marine biofilms against terrestrial phytopathogenic fungi. Some bacteria closely related to Bacillus mojavensis (three isolates) 

and Bacillus firmus (one isolate) displayed antagonistic activity against Colletotrichum gloeosporioides ATCC 42374, selected as first screen organism. The four isolates were further quantitatively tested 

against C. gloeosporioides, Colletotrichum fragariae, and Fusarium oxysporum on two culture media, potato dextrose agar (PDA) and a marine medium-based agar [yeast extract agar (YEA)] at different 

times of growth of the antagonists (early, co-inoculation with the pathogen and late). Overall antagonistic assays showed differential susceptibility among the pathogens as a function of the type of culture 

media and time of colonization (P < 0.05). In general, higher suppressive activities were recorded for assays performed on YEA than on PDA; and also when the antagonists were allowed to grow 24 h 

earlier than the pathogen. F. oxysporum was the most resistant fungus while the most sensitive was C. gloeosporioides ATCC 42374. Significant differences in antagonistic activity (P < 0.05) were found 

between the different isolates. In general, Bacillus sp. MC3B-22 displayed a greater antagonistic effect than the commercial biocontrol strain Bacillus subtilis G03 (KodiakA (R)). Further incubation 

studies and scanning electronic microscopy revealed that Bacillus sp. MC3B-22 was able to colonize, multiply, and inhibit C. gloeosporioides ATCC 42374 when tested in a mango leaf assay, showing 

its potential for fungal biocontrol. Additional studies are required to definitively identify the active isolates and to determine their mode of antifungal action, safety, and biocompatibility. 

Padghan, P. R. and M. M. Baviskar (2009). "Efficacy of bioagent and different root extracts for supression of chickpea wilt in vitro." Asian Journal of Bio Science 4(1): 56-58. 

udid, sorghum (Sorghum bicolor), groundnut and mung bean and biological control agents (Trichoderma viride, T. harzianum, T lignorum and T. koningii) against the chickpea wilt pathogen, Fusarium 

oxysporum f.sp. ciceris (FOC), was studied in the laboratory. A lower radial mycelial growth and a higher inhibitory effect were recorded in sorghum root extract medium (28.00 mm and 54.34%), 

respectively, however, it was at par with groundnut root extract medium (30.00 mm and 51.08%), compared to the control (61.33 mm). In dual culture technique, the growth of FOC was restricted by T. 

viride (56.16%), followed by T. harzianum (50.57%). T. lignorum recorded the minimum zone of inhibition (40.45%). 

Qiu, W., H. Huang, et al. (2009). "Screening of actinomycete against Fusarium oxysporum f. sp. cubense and identification of strain DA07408." Research of Agricultural Modernization 30(1): 126-128. 

samples, and 8 of these strains showed significant activities against F. oxysporum f.sp. cubense. One actinomycete (DA07408) isolated from an arboretum in Danzhou, Hainan, China, exhibited marked 

antagonism towards F. oxysporum f.sp. cubense. The conditions for the fermentation of the actinomycete were optimized. Based on the morphological, physiological and biochemical characteristics of 

the strain, and on the analysis of 16S rDNA and phylogenetic tree, DA07408 was identified as Streptomyces olivochromogenes. 

Raddadi, N., A. Belaouis, et al. (2009). "Characterization of polyvalent and safe Bacillus thuringiensis strains with potential use for biocontrol." Journal of Basic Microbiology 49(3): 293-303. 

Sixteen Bacillus thuringiensis (Bt) strains were screened for their anti-insect, antibacterial and antifungal determinants by phenotypic tests and PCR targeting major insecticidal proteins and complements, 

chitinases, lactonases, beta-1,3-glucanases and zwittermicin A. Six strains had genes of at least two major insecticidal toxins and of insecticidal complements. With regard to fungal biocontrol, all the 

strains inhibited Fusarium oxysporum and Aspergillus flavus growth and four strains had all or most of the antifungal determinants examined, with strain Bt HD932 showing the widest antifungal activity 

spectrum. Autolysins, bacteriocin and AHL-lactonases were produced by all or most of the tested strains with different activity spectra including pathogens like Listeria monocytogenes. Safety evaluation 

was carried out via PCR by screening the B. cereus psychrotolerance-related genes, toxin genes and the virulence pleiotropic regulator plcR. Diarrheal enterotoxins and other toxin genes were widespread 

among the collection with strains Bt HD9 and H45 lacking psychrotolerance-related genes, while five strains were positive. Only three strains (BMG1.7, H172, H156) resulted positive with primer sets 

targeting partial or complete plcR gene. By Vero Cell Assays, Bt HD868 followed by Bt HD9 were shown to be the safest strains. These polyvalent and safe Bt strains could be very promising in field 

application. 

Rasal, P. H., J. R. Shelar, et al. (2009). "Effect of endophytic antagonist on pigeonpea." Journal of Maharashtra Agricultural Universities 34(1): 52-53. 

resistant (ICP 8863) and resistant (BDN2) cultivars of pigeon pea were screened against Fusarium oxysporum f. udum [F. udum]. The inoculation of endophytic antagonists into different cultivars of 

pigeon pea improved germination, plant height, branching, nodulation, root length and biomass production, and reduced wilt intensity significantly over the un-inoculated control. Among the inoculants, 

Pseudomonas-2 was the most beneficial, followed by Pseudomonas-3, Bacillus-3, Pseudomonas-1, and Bacillus-1 and -2. Antagonists isolated from resistant cultivar were the most beneficial, followed 

by antagonists from the moderately resistant cultivar, and antagonists isolated from the susceptible cultivar. 

135


Recep, K., S. Fikrettin, et al. (2009). "Biological control of the potato dry rot caused by Fusarium species using PGPR strains." Biological Control 50(2): 194-198. 

In this study, a total of 17 Plant Growth Promoting Rhizobacteria (PGPR) strains, consisting of eight different species (Bacillus subtilis, Bacillus pumilus, Burkholderia cepacia, Pseudomonas putida, 

Bacillus amyloliquefaciens, Bacillus atrophaeus, Bacillus macerans and Flavobacter balastinium), were tested for antifungal activity in in vitro (on Petri plate) and in vivo (on potato tuber) conditions 

against Fusarium sambucinum, Fusarium oxysporum and Fusarium culmorum cause of dry rot disease of potato. All PGPR strains had inhibitory effects on the development of at least one or more fungal 

species on Petri plates. The strongest antagonism was observed in B. cepacia strain OSU-7 with inhibition zones ranging from 35.33 to 47.37 mm. All PGPR strains were also tested on tubers of two 

potato cultivars 'Agria' and 'Granola' under storage conditions. Only B. cepacia strain OSU-7 had significant effects on controlling potato dry rot caused by three different fungi species on the two potato 

cultivars. There were no significant differences in rot diameters among the treatments in comparison to the negative control (with water). This is the first study showing that B. cepacia has great potential 

to be used as effective biocontrol agent of Fusanium dry rot of potatoes (F. oxysporum and F culmorum) under storage conditions. (C) 2009 Elsevier Inc. All rights reserved. 

Riaz, T., S. N. Khan, et al. (2009). "Effect of co-cultivation and crop rotation on corm rot disease of Gladiolus." Scientia Horticulturae 121(2): 218-222. 

Field and pot experiments were conducted to evaluate the effect of co-cultivation and crop rotation on the growth and corm rot disease of gladiolus (Gladiolus grandiflorus sect. Blandus) cv. Aarti caused 

by Fusarium oxysporum f.sp. gladioli (Massey) Snyd. and Hans. In the field experiment, gladiolus was co-cultivated with 10 agricultural/horticultural crops viz. Allium cepa L., Brassica campestris L., 

Capsicum annuum L., Eruca sativa Mill., Helianthus annuus L., Tagetes erectus L., Zea mays L., Vinca rosea L. and Rosa indica L., in a soil infested with F. oxysporum. All the crops except V. rosea and 

R. indica reduced disease incidence. The effect of H. annuus and T. erectus was significant and more pronounced than other co-cultivated crops. In general, root and shoot dry biomass, corm fresh weight, 

number of cormlets and number of flowers per spike decreased as compared to the un-inoculated monoculture gladiolus treatment (negative control) but these parameters enhanced as compared to the F. 

oxysporum inoculated monoculture gladiolus treatment (positive control). In a pot experiment, all the crops of the field experiment except V. rosea and R. indica were sown in rotation with gladiolus. Pot 

grown plants of different species were harvested at maturity and the soil was inoculated with F oxysporum. Gladiolus was cultivated I week after inoculation. Disease incidence was significantly 

suppressed in all the treatments ranging from 29% to 53%. The highest suppression of disease incidence was recorded in T erectus (53%) followed by B. campestris (49%). The effect of preceding crops 

on various vegetative parameters was similar in the pot experiment to that of the field experiment. The present study suggests that corm rot disease of gladiolus can be managed by mixed cropping of H. 

annuus and T erectus or cultivation of T. erectus and B. campestris in rotation. (c) 2009 Elsevier B.V. All rights reserved. 

Saidi, N., S. Kouki, et al. (2009). "Characterization and selection of Bacillus sp strains, effective biocontrol agents against Fusarium oxysporum f. sp radicis-lycopersici, the causal agent of Fusarium crown 

and root rot in tomato." Annals of Microbiology 59(2): 191-198. 

The antagonistic activities of 20 Bacillus isolates were tested with dual culture and greenhouse conditions against Fusarium oxysporum f. sp. radicis-lycopersici (FORL) race 0, the causal agent of 

Fusarium crown and root rot of tomato. Under dual culture, 10 isolates inhibited mycelial growth > 38% and the most effective inhibited fungal growth > 50%. The 20 Bacillus isolates were tested for 

production of volatiles, cyanide, antibiotics, and phosphorus solubilisation; 15 isolates produced volatiles that inhibited growth of pathogens, 9 isolates produced cyanide, 10 produced antibiotics, and five 

solubilised phosphorus. Greenhouse experiments with the same 20 isolates revealed the effectiveness of 12 strains, which increased the percentage of healthy plants in the tested cultivar from 66 to 96%. 

The best disease control was achieved by isolates B11, B5, B17, and B18. However, B11 and B17 were the only isolates that produced cyanide, antibiotics, solubilised phosphate and showed 44% 

inhibition of fungal growth. The selected strains could be considered in plant growth promotion and biological disease control. 

Shi, Y. W., K. Lou, et al. (2009). "Isolation, quantity distribution and characterization of endophytic microorganisms within sugar beet." African Journal of Biotechnology 8(5): 835-840. 

The present investigation was undertaken in order to document the spectrum of endophytes colonizing healthy leaves of sugar beet cultivars in Xinjiang Province ( China) and to determine the degree of 

colonization at three growth stages. From the 360 sugar beet leaf and root segments incubated, 221 bacterial isolates, 34 fungal isolates and 5 actinomycete isolates were obtained. Of all the isolates, 7 

bacterial species and 6 fungal species were identified. The actinomycete isolates were characterized as Streptomyces griseofuscus and Streptomyces globisporus. There were significant differences 

between microorganisms, stages of growth, and stages of microorganism interaction. The number of microorganisms isolated increased during the growth period of the sugar beet. At the same time, the 

number of microorganisms affecting different parts of the sugar beet tissue was quite different. The greatest number of microorganisms was found in the secondary root emergence zone of the sugar beet 

tissue. Endophytic microorganisms in sugar beet promote growth and increase the yield of the beet. 

Son, S. H., Z. Khan, et al. (2009). "Plant growth-promoting rhizobacteria, Paenibacillus polymyxa and Paenibacillus lentimorbus suppress disease complex caused by root-knot nematode and fusarium wilt 

fungus." Journal of Applied Microbiology 107(2): 524-532. 

Paenibacillus strains against disease complex caused by Meloidogyne incognita and Fusarium oxysporum f. sp. lycopersici interactions. Methods and Results: Paenibacillus strains were collected from 

rotten ginseng roots. The strains were tested under in vitro and pots for their inhibitory activities, and biocontrol potential against disease complex caused by M. incognita and F. oxysporum f. sp. 

lycopersici on tomato. In in vitro experiments, among 40 tested strains of Paenibacillus spp., 11 strains showed antifungal and nematicidal activities against F. oxysporum f. sp. lycopersici and M. 

136

Appendix 6 

incognita, respectively. Paenibacilluspolymyxa GBR-462; GBR-508 and P. lentimorbus GBR-158 showed the strongest antifungal and nematicidal activities. These three strains used in pot experiment 

reduced the symptom development of the disease complex (wilting and plant death), and increased plant growth. The control effects were estimated to be 90-98%, and also reduced root gall formation by 

64-88% compared to the untreated control. Conclusion: The protective properties of selected Paenibacillus strains make them as potential tool to reduce deleterious impact of disease complex plants. 

Significance and Impact of the Study: The study highlights biocontrol potential of Paenibacillus strains in management of disease complex caused by nematode-fungus interaction. 

Srinivasan, K., G. Gilardi, et al. (2009). "BACTERIAL ANTAGONISTS FROM USED ROCKWOOL SOILLESS SUBSTRATES SUPPRESS FUSARIUM WILT OF TOMATO." Journal of Plant 

Pathology 91(1): 147-154. 

Five bacterial E,trains (FC-6B, FC-7B, FC-8B, FC-9B and FC-24B) isolated from used rockwool soilless substrates were identified using 16S ribosomal DNA (16S rDNA) sequence analysis as 

belonging to the Pseudomonas genus. Seven glasshouse trials were conducted in order to evaluate the efficacy of these bacteria strains (Pseudomonas putida FC-6B, Pseudomonas sp. FC-7B, 

Pseudomonas putida FC-8B, Pseudomonas sp. FC-9B and Pseudomonas sp. FC-24B) together with Achromobacter sp. AM1 and Serratia sp. DM1 obtained from suppressive sod, against Fusarium wilt 

of tomato. Two commercial bioproducts, Trichoderma harzianum T22 (RootShield) and Pseudomonas chlororaphis MA 342 (Cedomon) were also evaluated. Different treatment strategies including soil 

application (10(7) and 10(8) cfu ml(-1)) were adopted in different glasshouse trials (Trial I to VI) to test the efficacy of the bacterial strains against Fusarium wilt. Root dipping was used in Trial VII 

(10(8) and 10(9) cfu ml(-1)). The lowest: disease incidence (3.3) was recorded with a single application of P. putida FC-6B at 10(8) cfu ml(-1). Similar results were obtained with the same bacteria when 

the concentration was decreased to 10(7) cfu ml(-1) but an increasing number of applications was required. The highest plant biomass (50.3 g/plant) was recorded in the P. putida FC-8B treatment (Trial 

III). In conclusion, the current study showed the potential biocontrol activity of bacterial strains FC-6B, FC-7B, FC-8B, FC-9B and FC-24B isolated from re-used rockwool soilless substrates against 

Fusarium wilt disease, and the growth promoting activity of these strains on tomato plants. 

Srivastava, D. K., A. K. Singh, et al. (2009). "Efficacy of bio-control agents and seed dressing fungicides against damping off of tomato." Annals of Plant Protection Sciences 17(1): 257-258. 

in Unao, Madhya Pradesh, India, during 2005-06 yielded associated pathogen on PDA medium. The antagonistic activity of biological control agents against Fusarium oxysporum f.sp. lycopersici was 

determined using dual culture method. All the antagonists and fungicide inhibited the mycelial growth of Fusarium, however, Trichoderma viride caused maximum inhibition of mycelial growth. 

Trichoderma viride, Trichoderma harzianum, Gliocladium virens, carbendazim and thiram, which showed significant in vitro inhibition of Fusarium were tested in the field. Maximum increase in seed 

germination (83.4%), seedling survival (79.0) and plant height (6.32 cm) over the control was observed when treated with Trichoderma viride followed by Trichoderma harzianum, carbendazim, thiram, 

and Gliocladium virens. 

Thanh, D. T., L. T. T. Tarn, et al. (2009). "Biological Control of Soilborne Diseases on Tomato, Potato and Black Pepper by Selected PGPR in the Greenhouse and Field in Vietnam." Plant Pathology Journal 

25(3): 263-269. 

Bacterial wilt, Fusarium wilt and Foot rot caused by Ralstonia solanacearum, Fusarium oxysporum, and Phytophthora capsici respectively, continue to be severe problems to tomato, potato and black 

pepper growers in Vietnam. Three bio-products, Bacillus vallismortis EXTN-1 (EXTN-1), Bacillus sp. and Puenibacillus sp. (ESSC) and Bacillus substilis (MFMF) were examined in greenhouse 

bioassay for the ability to reduce bacterial wilt, fusarium wilt and foot rot disease severity. While these bio-products significantly reduced disease severities, EXTN-1 was the most effective, providing a 

mean level of disease reduction 80.0 to 90.0% against bacterial wilt, fusarium wilt and foot rot diseases under greenhouse conditions. ESSC and MFMF also significantly reduced fusarium wilt, bacterial 

wilt and foot rot severity under greenhouse conditions. Bio-product, EXTN-1 with the greatest efficacy under greenhouse condition was tested for the ability to reduce bacterial wilt, fusarium wilt and 

foot rot under field condition at Song Phuong and Thuong Tin locations in Ha Tay province, Vietnam. Under field condition, EXTN-1 provided a mean level of disease reduction more than 45.0% 

against all three diseases compared to water treated control. Besides, EXTN-1 treatment increased the yield in tomato fruits 17.3% than water treated control plants. 

Wu, H., X. Yang, et al. (2009). "Suppression of Fusarium wilt of watermelon by a bio-organic fertilizer containing combinations of antagonistic microorganisms." BioControl 54(2): 287-300. 

the crop has been grown for many seasons. Its occurrence results in a severely decreased watermelon crop. The goal of this study was to assess the capability of a new product (bio-organic fertilizer) to 

control the wilt in Fusarium-infested soil. Pot experiments were conducted under growth chamber and greenhouse conditions. The results showed that the fertilizer controlled the wilt disease. Compared 

with control pots, the incidence rates of Fusarium wilt at 27 and 63 days following treatment of the plants with the bio-organic fertilizer at a rate of 0.5% (organic fertilizer+antagonistic microorganisms, 

including 3*109 CFU g-1 respectively, in both the growth chamber and greenhouse settings. The activities of antioxidases (catalase, superoxide dismutase and peroxidase) in watermelon leaves increased 

by 38.9, 150 and 250%, respectively. In the roots, stems and leaves, the activity of beta-1,3-glucanase (pathogenesis-related proteins) increased by 80, 1140 and 100% and that of chitinase increased by 

240, 80, and 20%, respectively, while the contents of malondialdehyde fell by 56.8, 42.1 and 45.9%, respectively. These results indicate that this new fertilizer formula is capable of protecting 

watermelon from Fusarium oxysporum f.sp. niveum. The elevated levels of defense-related enzymes are consistent with the induction and enhancement of systemic acquired resistance of plant. 

137


Wu, Q., H. Zeng, et al. (2009). "Stability of fermentation broth of actinomycete strain WZ162 resistance to Fusarium oxysporum f.sp. cubense of banana." Guangxi Agricultural Sciences 40(4): 366-369. 

The fermentation broth of actinomycete strain WZ162 has strong inhibiting effect against Fusarium oxysporum f.sp. cubense of banana. Under different conditions, the stabilities of fermentation broth of 

WZ162 were detected. The results showed that the fermentation broth of WZ162 had better heat stability when temperature of water bath was below 80C. The antibiotics ingredient of fermentation broth 

would not be changed and can maintain the antifungal activity under conditions of sun light and ultraviolet rays. Under acid and neutrality conditions, the inhibition rate of fermentation broth against 

Focr4 was 24.92%-34.73% and 11.21%-25.39%, respectively. Therefore, the stability of fermentation broth in acid was better than that of neutrality. When the fermentation broth with pH 1-12 were 

treated with different time in 100C water bath, the inhibition rate was obviously lower than that of the treatments without water bath, and the stability of fermentation broth with pH 1 was the best. 

Yin, X., D. Chen, et al. (2009). "An endophytic Erwinia chrysanthemi strain antagonistic against banana fusarium wilt disease." Chinese Journal of Biological Control 25(1): 60-65. 

An endophytic strain E353 was obtained from the pseudostem of healthy banana plant in a field heavily infected with Fusarium oxysporum f. sp. cubense (FOC). Antagonism of the strain against FOC 

was tested via dual-culture, inhibition test on conidia germination, and pot trials. Results showed that E353 effectively inhibited mycelium growth and conidia germination. Efficacy of strain E353 to 

control the wilt disease was 60.67% in pot trials. Strain E353 was identified as Erwinia chrysanthemi according to its characteristics in morphology, physiology, biochemistry and 16S rDNA sequence. 

Zhong, X., M. Liang, et al. (2009). "Study on the inhibition of Trichoderma sp. against Fusarium oxysporum f. sp. cubense in banana." Journal of Fruit Science 26(2): 186-189. 

effective antagonist against Fusarium oxysporum f. sp. cubens, was isolated and identified as Trichoderma sp. based upon 18S rDNA gene analysis. With solid and liquid cultures, the inhibitive efficacy 

to the growth of Fusarium oxysporum f. sp. cubens was primarily studied. The experimental results showed that the cells of Fusarium oxysporum f. sp. cubens were completely covered by short fiber-like 

hyphace and spore stem of G2 within 7 days in the dual culture plate, and in the antagonist plate, the average rate of inhibitory by the culture solution of G2 was about 90.4%, the average rate of the 

inhibitory by volatile substance reached 68.3%. After 10 days' incubation with 20% (v/v) fungal strain G2, the melt of the pathogenic mycel and spore were observed in the liquid culture containing 

1.0*107 cfu . L-1 G2 can strongly inhibit the growth of Fusarium oxysporum f. sp. cubens. 

Zhu, H., Y. Ma, et al. (2009). "Control effect of combining biocontrol strains against Fusarium oxysporium f. sp. niveum and Verticillium dahliae." Journal of Northwest A & F University - Natural Science 

Edition 37(7): 152-156. 

Objective: Five actinomycetes strains having certain inhibiting capability were screened as material to study the control effect of the actinomycetes and five combinations on watermelon Fusarium wilt 

and Eggplant Verticillium wilt, and to filter the combining biocontrol strains which have better biocontrol efficacy and growth promotion. Method: The biocontrol efficacy and growth promotion of 

single and combining strains were analyzed by antagonistic activity in vitro and manual inoculation in vivo. Result: Strain SC11 and SE2 had significant inhibiting effect on Fusarium oxysporium f. sp. 

niveum and Verticillium dahliae in vitro. Inhibiting rate on conidia germination was also high; in greenhouse experiment, 84.93% control ratio to Fusarium oxysporium f. sp. niveum and 71. 48% to 

Verticillium dahliae were found by C2; The fermentation broth of C3 had the most significant effect for every index of watermelon. The effect on reduction intensity of watermelon rootage was obvious. 

For eggplant, the growth promotion was only inferior to strain SF6. Conclusion: These results suggested that the control effect and growth promotion of combining biocontrol strains are significantly 

higher than individual, and combining strains express complementary biocontrol activities by collaboration. There is no correlation between the number of strains and control effect, only proper 

combinations of biocontrol strains can enhance disease control effect. 

138

Appendix 7. Number of references retrieved by using the CAB Abstracts database in 

order to review scientific literatures on augmentative biological control in 

selected crops for Chapter 2. 

GRAPEVINE* 

Key words 1973-2008 1998-2008 

Biological control 1644 - 





Insects biological control 773 373 

Mites biological control 320 190 

Total references dealing with 

augmentative biocontrol to be examined 

607 579 

* Survey includes records for grapevine, grape and vineyard. 

APPLE 

Key words 1973-2008 1998-2008 










1145 1099 

PEAR 

Key words 1973-2008 1998-2008 










400 391 

139

140 Nicot et al. (Appendix for Chapter 1) 

CORN* 

Key words 1973-2008 1998-2008 










1919 1805 

* Survey include records for corn and maize. 

WHEAT 

Key words 1973-2008 1998-2008 










980 949 

CARROT 

Key words 1973-2008 1998-2008 










76 73 

ONION 

Key words 1973-2008 1998-2008 










313 304 

140

Appendix 8. Collection of data on augmentative biological control of pests in grapevine. Each table refers to a group of biocontrol agents. 

8.1 Parasitoid Hymenoptera: Trichogramma spp. (Trichogrammatidae) [10 species] 

References 

Species of 

biocontrol agent 

Species of insect pest Taxonomic 

category of 

Remund & Bigler, 1986 T. dendrolimi Eupoecilia ambiguella 


pests 

Lepidoptera: 

Tortricidae 

Country 

Type of 

augmentation 

Type of 

test 

Lab 

Efficacy of 

biocontrol 

agents* 

Additional information and 

results 

Evaluation of biological 

parameters 

Switzerland Field Evaluation of biological 

parameters 

T. maidis Switzerland Inundative Field + 

Segonca & Leisse, 1989 T. semblidis Eupoecilia ambiguella and Lepidoptera: Ahr Valley, Inundative Field + 


Tortricidae Germany 

Glenn & Hoffmann, 1997 T. carverae Epiphyas postvittana 


Lepidoptera: 

Tortricidae 

Victoria, 

Australia 

Inundative Field 

(small 

+ 

Basso et al., 1998 

Basso et al., 1999 

Garnier-Geoffroy et al., 

1999 

Hommay et al., 2002 

T. pretiosum 

T. exiguum 

Argyrotaenia sphaleropa 

(South American tortricid 

moth), 

Bonagota cranaodes 

(Brasilian apple leafroller) 

A. sphaleropa 

B. cranaodes 

Lepidoptera: 

Tortricidae 

T. pretiosum 

T. exiguum 

Lepidoptera: 

Tortricidae 

T. brassicae Lobesia botrana Lepidoptera: 

Tortricidae 

T. evanescens and Lobesia botrana 

Lepidoptera: 

T. cacoeciae (two 

Tortricidae 

strains) 

Nagargatti et al., 2002 T. minutum Endopiza viteana (grape 

berry moth) 

Lepidoptera: 

Tortricidae 

Thomson & Hoffmann, 

2002 

T. carverae Epiphyas postvittana 


Lepidoptera: 

Tortricidae 

Nagargatti et al., 2003 T. minutum Endopiza viteana Lepidoptera: 

Tortricidae 

Zimmermann, 2004 Trichogramma spp. Lobesia botrana and Lepidoptera: 

Eupoecilia ambiguella Tortricidae 

Begum et al., 2006 T. carverae Epiphyas postvittana Lepidoptera: 

Tortricidae 

blocks) 

Uruguay Lab Evaluation of biological 

parameters 

Uruguay Inundative Field + 

Lab - Evaluation of allelocemical 

relations 

France Inundative Field + + as % parasitization. 

- - as % grapes attacked. 

Pennsylvania, 

USA 

Field + + as natural parasitism. 

Inundative releases of T. 

minutum in border rows is 

suggested 

Lab 

Assessment of quality indicators 

Field 

Inundative Field + Parasitoids released in border 

rows 

Victoria, 

Australia 

Pennsylvania, 

USA 

Germany Inundative Field Commercialized to be used in 

home garden 

Australia Inundative Greenho + Ground-cover plant species 

use/ 

identified to improve performance 

Field 

of mass released parasitoids. 

141

Giorgini (Appendix for Chapter 2) 

El-Wakeil et al., 2008 T. evanescens Lobesia botrana (European 

grape berry moth) 

* + means effective, - means not effective biocontrol agent. 

Lepidoptera: 

Tortricidae 

Egypt Inundative Field + Parasitism > 97% and reduction 

percents of infestation reached 

96.8% 

8.2 Parasitoid Hymenoptera: Encyrtidae [4 species], Pteromalidae [1 species] 

Reference 

Species of 

biocontrol agent 

Species of insect 

pest 

Taxonomic category of 

pests 

Walton & Pringle, 1999 

Walton & Pringle, 2004 

Abd-Rabou, 2005 

Daane et al., 2006 


Kapongo et al., 2007 

Coccidoxenoides 

peregrinus 

(Encyrtidae) 

Coccidoxenoides 

perminutus 

(Encyrtidae) 

Anagyrus kamali 

(Encyrtidae) 

Anagyrus 

pseudococci 

(Encyrtidae) 

Anagyrus 

pseudococci 

(Encyrtidae) 

Muscidifurax 

raptor 

(Pteromalidae) 

Planococcus ficus 

(vine mealybug) 


(vine mealybug) 

Maconellicoccus 

hirsutus 



Ceratitis capitata 

(Mediterranean fruit 

fly) 


Hemiptera: 


Hemiptera: 


Hemiptera: 


Hemiptera: 


Hemiptera: 


Cuontry 

Type of 

augmentation 

Type of 

test 

Efficacy of 


agents* 


results 

South Africa Lab Compatibility of fungicides and 

incompatibility of insecticides 

with augmentative releases 

South Africa Inundative Field + Mass release was at least as 

effective as the chemical control 

Egypt Inundative Field + It is concluded that the releases of 

parasitoids were suitable for 

control. 

California Inoculative Field + Promising results. Commercial 

products are not yet available. 

Israel Inoculative Field + Promising results. Commercial 

products are not yet available. 

Diptera: Tephritidae Canada Inundative Field 

Lab 

cages 

+ M. raptor constitutes a promising 

biocontrol agent in vineyards. 

8.3 Predators of mites. Acari: Phytoseidae. 

References Species of biocontrol 

agent 

Species of mite pest 

Boller et al., 1988 Typhlodromus pyri Panonychus ulmi, 

Tetranychus urticae 

Taxonomic 

category of 

pests 

Acari: 

Tetranychidae 

Country 

Type of 

augmentation 

Type of 

test 

Efficacy of 


agents* 


results 

Switzerland Inoculative Field Inoculative release of T. pyri 

along with the increase of the 

internal ecological diversity 

achieved by proper management 

of the green cover plants will 

have a strong influence on 

predator densities. 

142

Appendix 8 

Camporese & Duso, 1996 

Typhlodromus pyri, 

Amblyseius andersoni, 

Kampimodromus aberrans 

Panonychus ulmi 

Acari: 

Tetranychidae 

Takahashi et al., 1998 Phytoseiulus persimilis Tetranychus kanzawai Acari: 

Tetranychidae 

Duso & Vettorazzo, 1999 

Kampimodromus 

aberrans, Typhlodromus 

pyri 

Panonychus ulmi, 

Eotetranychus carpini 

Calepitrimerus vitis 

Acari: 

Tetranychidae 

Acari: 

Eriophyidae 

Marshall & Lester, 2001 Typhlodromus pyri Panonychus ulmi Acari: 

Tetranychidae 

Duso et al., 2006 

Typhlodromus pyri 

strain resistant to 

organophosphates 

Panonychus ulmi, 

Eotetranychus carpini 

Calomerus vitis 


Acari: 

Tetranychidae 

Acari: 

Eriophyidae 

Italy Inoculative Field + Different colonization patterns on 

three grape varieties (with 

different pubescent leaf 

undersurfaces). 

The high competitiveness of K. 

aberrans over the other 2 

phytoseid species is a major 

factor in selecting predatory 

species for inoculative releases. 

Japan Inundative Field 

(grape in 

green 

house) 

+ Release of P. persimilis onto the 

grass ground cover in the spring. 

No chemical control was 

required. 

Veneto, Italy Inoculative Field (A) + Releases were successful and the 

predators became more abundant 

on the variety with pubescent leaf 

under-surface. 

Native A. andersoni were 

displaced by T. pyri. 

Field (B) + Two grape varieties with different 

leaf hair density. 

T. pyri colonization failed; K. 

aberrans was more successful on 

glabrous varieties. K. aberrans 

displaced native P. finitimus. 

Ontario, 

Canada 

North-eastern 

Italy 

Inoculative Field + T. pyri out-competed native 

Amblyseius fallacies. 

T. pyri is an effective biocontrol 

agent and may be introduced by 

transferring leaves. 

Inoculative Field 15-years observations. The 

predator colonized the vineyard 

and competed successfully with 

other species. 

Role of alternative foods, leaf 

morphology and selective 

pesticides. 

143


8.4 Predators of insects. Neuroptera: Chrysopidae [3 species] and Coleoptera: Coccinellidae [2 species] 

Reference 


Daane & Yokota, 1997 

Wunderlich & Giles, 

1999 

Species of biocontrol 

agent 

NEUROPTERA: 

CHRYSOPIDAE 

Chrysoperla carnea 

(common green 

lacewing) 

Chrysoperla carnea, 

C. comanche, 

C. rufilabris 

Chrysoperla rufilabris 

Species of 

insect pest 

Erythroneura 

variabilis, 

E. elegantula 

(leafhoppers) 

Erythroneura 

variabilis, 

E. elegantula 

(leafhoppers) 

Erythroneura 

variabilis, 

E. elegantula 

(leafhoppers) 

COLEOPTERA: 

COCCINELLIDAE 

Anagnou et al., 2003 Nephus includens Planococcus 

citri 


Cryptolaemus 

montrouzieri 

Pseudococcus 

maritimus, 

P. longispinus 

(mealybugs) 

Mani, 2008 

Cryptolaemus 

montrouzieri 

Planococcus 

citri 


Taxonomic 

category of pests 

Hemiptera: 

Cicadellidae 

Hemiptera: 

Cicadellidae 

Hemiptera: 

Cicadellidae 

Hemiptera: 


Hemiptera: 


Hemiptera: 


Country 

Type of 

augmentation 

Type of test 

California Inundative Field 

(caged smallplot) 

Field 

(uncaged 

small-plot) 

Field 

(on-farm 

trials) 

Efficacy of 


agents* 

Additional information and results 

- Average leafhopper density reduction 

29.5%. 

- Release rates reflecting commercial 

recommendations. 

Average reduction 15.5%. 

- Average reduction 9.6% 

Not sufficient to lower the leafhopper 

density below the economic injury 

threshold. 

California Inundative Field - Aspects of release strategies evaluated. 

High mortality of lacewing eggs and 

neonate larvae. 

California Inundative Field A mechanical technique was assessed for 

releasing eggs in liquid suspensions. 

Adhesion of eggs to the canopy was an 

issue. 

Greece Field It is suggested, for combined infestation 

by L. botrana and mealybugs, the 

application of B. thuringiensis and the 

releases of the effective predator N. 

includens. 

California Inoculative Field Commonly released in vineyards, but 

release rates, timing, and expected 

outcomes have not been scientifically 

evaluated. 

It may be best used by releasing at hot 

India Inundative Green 

house 

+ 

spots where the mealybug density is high. 

144

Appendix 8 

8.5 Fungi [5 species] 

Reference 

Berner & 

Schnetter, 2002 

Tsitsipis et al., 

2003 

Species of biocontrol 

agent 

Beauveria brongniartii 

(in combination with the 

nematode H. 

bacteriophora) 

Beauveria bassiana 

Species of insect pest 

Melolontha melolontha 

(European cockchafer) 

Frankliniella 

occidentalis 

(western flower thrips) 

Taxonomic 

category of pests 

Coleoptera: 

Scarabeidae 

Thysanoptera: 

Thripidae 

Al-Jboory et al., 

2006 

Beauveria bassiana grape thrips Thysanoptera: 

Thripidae 

Lopes et al., 2002 Metarhizium anisopliae Frankliniella 

Thysanoptera: 

occidentalis 

Thripidae 

Laengle et al., 

2004 

Kirchmair et al., 

2004 


2005 

Huber & 

Kirchmair, 2007 

Metarhizium anisopliae 




Daktulosphaira 

vitifoliae 



vitifoliae 



vitifoliae 



vitifoliae 


Hemiptera: 

Phylloxeridae 

Hemiptera: 

Phylloxeridae 

Hemiptera: 

Phylloxeridae 

Hemiptera: 

Phylloxeridae 

Country 

Type of 

augmentation 

Type of 

test 

Germany Inundative Field 

(soil) 

Efficacy of Additional information and results 


agents* 

+ Only under optimum conditions and with 

high doses control of the white grubs 

could be reached. 

Greece Inundative Field + 

- 

B. bassiana in combination with mass 

trapping was compared to mass trapping 

or insecticides. 

Less efficient in the control of insect 

population if compared to some 

chemicals. 

Iraq Lab + Two isolates of B. bassiana showed 

100% mortality after 5 days 

Brazil Inundative Field + The effect of chemicals (thiacloprid and 

methiocarb) with or without M.a. was 

tested. M.a. in combination with 

methiocarb was the best strategy. 

Austria Inundative Field Non-target effects on soil fauna: no 

negative effects detected. 

Austria Inundative Lab + M.a. was effective in pot experiments. 

Potential role of M.a. in grape phylloxera 

control. 

Germany Inundative Field + M.a. was effective. 

No target effects on soil fauna (Acari, 

Collembola, Lumbricida and the 

Carabidae Harpalus affinis) and fungi. 

Germany Inundative Field - Evaluation of efficacy: more difficulties 

arise in testing the efficacy of M.a. under 

field conditions because of the uneven 

distribution of roots and pest insects in 

the soil. 

145



2007 

Maheshkumar- 

Katke & Balikai, 

2008 


Metarhizium anisopliae, 

Verticillium lecanii, 

Clerodendron inerme 


vitifoliae 


Maconellicoccus 

hirsutus 

(grape mealybug) 


Hemiptera: 

Phylloxeridae 

Hemiptera: 


Germany Inundative Field + 3 months after application an increase of 

the M.a. density in soil was observed. 

Compared with untreated plots a lower 

infestation was observed in the M.a.- 

treated plots. Two years after treatment a 

control effect was still observed whereas 

the density of M.a. in soil decreased. 

Three years after treatment no effect on 

the pest was detectable and the M.a. 

density had decreased to a value similar 

to that in the control . A periodically 

application is necessary. 

India Inundative Field + 

8.6 Nematodes [5 species] 

Reference Species of biocontrol agent Species of insect pest Taxonomic 

category of 

pests 

Saunders & All, 

1985 

English-Loeb et 

al., 1999 

Steinernema carpocapsae 

Heterorhabditis 

bacteriophora 

(Oswego strain), 

Steinernema glaseri 

(isolate 326) 

Vitacea polistiformis 

(grape root borer) 

Daktulosphaira vitifolia 

(grape phylloxera - root 

form) 

Lepidoptera: 

Sesiidae 

Hemiptera: 

Phylloxeridae 

Country Type of augmentation Type 

of test 

Georgia, 

USA 

NY, 

USA 

Inundative 

(soil) 

Lab, 

Field 

Efficacy of 


agents* 

Lab + 


results 

+ Susceptibility of V.p. 1st-instar 

larvae. Augmentation of nematode 

populations during the critical 

period of V.p. oviposition and 

eclosion is suggested as a control 

technique. 

- 

- 

H. bacteriophora: reduced survival 

of attached phylloxera by up to 

80%. 

S. glaseri had no measurable impact. 

No evidence that H.b. could 

successfully reproduce within the 

bodies of the hosts. 

Augmentative use in the field in an 

release programme may be 

constrained by the need to use high 

densities, their dependence on moist 

soils, and their inability to propagate 

themselves within hosts. 

146

Appendix 8 

Berner & 

Schnetter, 2002 

Williams et al., 

2002 


bacteriophora, 

H.bacteriophora 

+ Beauveria brongniartii 

(fungus) 



H. zealandica, 

H. marelata, and 


Melolontha melolontha 

(European cockchafer) 

Vitacea polistiformis 

(grape root borer) 

Coleoptera: 

Scarabeidae 

Lepidoptera: 

Sesiidae 

Germany 

Inundative 

(soil) 

Ohio, USA Inundative Lab 

Field + Only under optimum conditions and 

with high doses of nematodes 

control of grubs could be reached. 

New variant for the application of 

nematodes proposed. 

Greenh 

ouse 

+ 

+ 

H. bacteriophora strains GPS11 and 

Oswego, H. zealandica strain X1, 

and H. marelata. 

S. carpocapsae strain All less 

effective 

H. zealandica strain X1 

H. bacteriophora strain GPS11 


8.7 Bacillus thuringiensis 

Reference 

B. thuringiensis 

subspecies 

Species of Insect 

pest 

Taxonomic 

category of 

pests 

Lepidoptera: 

Caroli et al., 1998 subsp. aizawai Lobesia botrana 

(grape berry moth) Tortricidae 

Keil & Schruft, 1998 

L. botrana, 

Lepidoptera: 

Eupoecilia 

Tortricidae 

ambiguella 

(grape berry moths) 

Morando et al., 1998 

L. botrana, 

Lepidoptera: 

E. ambiguella Tortricidae 

Boselli et al., 2000 L. botrana Lepidoptera: 

Tortricidae 

Fretay & Quenin, 2000 L. botrana Lepidoptera: 

Tortricidae 

Bagnoli & Lucchi, subsp. kurstaki Cryptoblabes Lepidoptera : 

2001 

gnidiella 

Pyralidae 

Boselli & Scannavini, 

2001 

Neves & Frescata, 

2001 

subsp. kurstaki 

subsp. aizawai 

(honey moth) 

L. botrana Lepidoptera: 

Tortricidae 

kurstaki x aizawai L. botrana Lepidoptera: 

Tortricidae 

Country Type of test Efficacy Additional results and information 

Emilia- 

Romagna, Italy 

Field + 90-95% reduction in damage against severe pest infestations 

comparable to the standard chemical products. 

Lab 

4 Bt products (0.2% Bactospeine FC, 0.1 % Delfin, 0.1% Dipel 

ES and 0.1% Thuricide HP) were compared. The influence of 

temperature on the efficacy is discussed. 

Toscana, Italy Field + 

Piemonte, Italy Field + The efficacy of Bt was compared to 7 insecticides. All the 

tested insecticides had a significantly good efficacy. 

Emilia- Field 

Bt compared to insecticides. 


France Field Evaluation of new formularions. 

Emilia- 


Bairrada, 

Portugal 

Field 

Treatments included Agree (Bt kurstaki and aizawi), 

flufenoxuron, chlorpyrifos, lufenuron, tebufenozide, 

methoxyfenozide, indoxacarb and spinosad. The best control 

was obtained with methoxyfenozide, indoxacarb, and spinosad. 

Field + TUREX was tested to control the L. botrana third generation. 

Great interest of this Bt product regarding its efficiency and 

persistence based in a correct spray moment determination. 

147


Anagnou et al., 2003 

Ifoulis & Savopoulou- 

Soultani, 2003 


subsp. aizawai 


Tortricidae 


Tortricidae 

Roditakis, 2003 L. botrana Lepidoptera: 

Tortricidae 

Samoilov, 2003 

Sparganothis 

pilleriana (grape 

leafroller) 

Lepidoptera: 

Tortricidae 

Bakr, 2004 subsp. kurstaki Lobesia botrana Lepidoptera: 

Tortricidae 

Besnard et al., 2004 subsp. aizawai Lobesia botrana Lepidoptera: 

Tortricidae 

Hera et al., 2004 subsp. kurstaki Hyphantria cunea Lepidoptera: 

(fall webworm) Arctiidae 

Laccone et al., 2004 subsp. kurstaki Lobesia botrana Lepidoptera: 

Tortricidae 

Mazzocchetti et al., 

2004 

Moiraghi et al., 2004 


L. botrana 

E. ambiguella 

Lepidoptera: 

Tortricidae 

Lepidoptera: 

Tortricidae 

Delbac et al., 2006 Lobesia botrana Lepidoptera: 

Tortricidae 

Marchesini et al., 2006 subsp. aizawai Lobesia botrana Lepidoptera: 


Tortricidae 

Laccone, 2007 Lobesia botrana Lepidoptera: 

Tortricidae 

Mescalchin, 2007 Lobesia botrana Lepidoptera: 

Tortricidae 

Mitrea et al., 

subsp. kurstaki Lobesia botrana Lepidoptera: 

2007 

Tortricidae 

Lab + Several products incorporated into an artificial diet resulted in 

>90% larval mortality. 

The same formulations did not significantly affect the survival 

of Nephus includens. 

Greece Field + Two formulations of Bt are significantly more effective than the 

control, the dusting being more effective in most cultivars and 

the spraying in a few cultivars. 

Greece Field Pest control strategy involves B.t. application, mating 

disruption, botanical insecticides and minimal use of 

insecticides 

Odessa, Ukraine Field + 

Egypt Field + The addition of sugar as a feeding stimulant to a 50% reduced 

rate of Dipel-2X resulted in higher control rates (80%) 

compared to using the recommended field rates of Dipel-2X 

alone or Actellic [pirimiphos-methyl]. 

France Field + Xen Tari commercial product. 

Romania Field + Dipel 2x WP at 0.075% also showed good protection. The 

synergenism of mixtures (50:50) of chemical and biological 

insecticides was effective in controlling the pest. 

Calabria, Italy Field + Bt gave satisfactory control if applied at the onset of 

ovideposition and provided the canopy was managed in such a 

way as to expose the berries. 

Abruzzo, Italy Field Mating disruption was compared with the traditional methods 

generally used in the area: chemicals (phosphorganic 

molecules) and B. thuringiensis. 

Italy Field - In four years, trials were carried out using several commercial 

products (9 insecticides and Bt). The best control was obtained 

using insecticides. Control was lower for azadirachtin and less 

constant for etofenprox and B. thuringiensis. 

France Field + L. botrana was well-controlled by the use of B.t. or IGR’s, 

without mating disruption justification 

Veneto, Italy Field + Bta compared to Btk and chemicals. 

Molise and 

Calabria, Italy 

Field 

High efficacy of B.t. aizawai. 

Pest control with indoxacarb, spinosad and B. thuringiensis 

applied against the 2nd generation of insects parasitizing fruit is 

also outlined 

Trentino, Italy Field + 5-years study (2000-2005). Formulations based Bt can be used 

for controlling tortricids such as L. botrana. 

Romania Field + Chemical insecticides followed by Btk to control the second or 

the third generation. Efficiency of the control treatments ranged 

between 89.4% and 91.4%. 

148

Appendix 8 

Morandi-Filho et al., 

2007 

Pryke & Samways, 

2007 

Ruiz-de-Escudero et 

al., 2007 


Argyrotaenia 

sphaleropa (South 

American tortricid 

moth) 

Epichoristodes 

acerbella 

(South African 

carnation tortrix) 


Lepidoptera: 

Tortricidae 

Lepidoptera: 

Tortricidae 

Lepidoptera: 

Tortricidae 

Subic, 2007 subsp. kurstaki Lobesia botrana Lepidoptera: 

Tortricidae 

Dongiovanni et al., subsp. kurstaki Lobesia botrana Lepidoptera: 

2008 

Tortricidae 

Brazil 

Lab 

Field 

+ 

+ 

Lab: reducition of the insect population by more than 90%. 

Field: reduced damage between 83.3 and 94.4%. The control 

efficacy of B.t was equal to that of chemicals. 

South Africa Field + DiPelReg commercial formulation 

Lab + The potential of Bt Cry proteins to control L. botrana was 

explored. 

Either Cry1Ia or Cry9C could be used in combination with 

Cry1Ab to control this pest, either as the active components of 

Bt sprays or expressed together in transgenic plants. 

Croatia Field + Over 90% control was achieved. 

Puglia, Italy Field + 

References 

Abd-Rabou S. 2005. The effect of augmentative releases of indigenous parasitoid, Anagyrus kamali (Hymenoptera: Encyrtidae) on populations of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in 

Egypt. Archives of Phytopathology and Plant Protection 38: 129-132. 

Al Jboory I.J., Ismail I.A. & Al Dahwe S.S. 2006. Evaluation of two isolates of Beauveria bassiana (Bals.) Vuill. against some insects and mites and testing the efficiency of some culture media. 

University of Aden, Journal of Natural and Applied Sciences 10(1): 23-29. 

Anagnou M., Kontodimas V. & Kontodimas D.C. 2003. Laboratory tests of the effect of Bacillus thuringiensis on grape berry moth Lobesia botrana (Lepidoptera: Tortricidae) and on the pseudococcids' 

predator Nephus includens (Coleoptera: Coccinellidae). Bulletin OILB/SROP 26(8): 117-119. 

Bagnoli B. & Lucchi A. 2001. Bionomics of Cryptoblabes gnidiella (Milliere) (Pyralidae Phycitinae) in Tuscan vineyards. Bulletin OILB/SROP 24(7): 79-83. 

Bakr H.A. 2004. A feeding stimulant for improving the efficacy of Bacillus thuringiensis var. kurstaki in larval control of the grape moth, Lobesia botrana Den. & Schiff. (Lepidoptera: Tortricidae). 

Egyptian Journal of Biological Pest Control 14(2): 411-413. 

Basso C., Grille G., Pompanon F., Allemand R. & Pintureau B. 1998. Comparison of biological and ethological characters of Trichogramma pretiosum and T. exiguum (Hymenoptera: Trichogrammatidae). 

Revista Chilena de Entomologia 25: 45-53. 

Basso C., Grille G. & Pintureau B. 1999. Efficiency of Trichogramma exiguum Pinto & Platner and T. pretiosum Riley to control Argyrotaenia sphaleropa (Meyrick) and Bonagota cranaodes (Meyrick) in 

Uruguayan vineyard. Agrociencia Montevideo 3(1): 20-26 

Begum M., Gurr G.M., Wratten S.D., Hedberg P.R. & Nicol H.I. 2006. Using selective food plants to maximize biological control of vineyard pests. Journal of Applied Ecology 43: 547-554. 

Besnard Y. & Boudet M. 2004. Bacillus thuringiensis sp. aizawai? Insecticide against grape berry moths and noctuids. Phytoma 575: 46-47. 

Berner M. & Schnetter W. 2002. Field trials with the entomopathogenic nematode Heterorhabditis bacteriophora against white grubs of the European cockchafer (Melolontha melolontha) in the southern 

part of Germany. Bulletin OILB/SROP 25(7): 29-34. 

Boller E.F., Remund U. & Candolfi,-M.P. 1988. Hedges as potential sources of Typhlodromus pyri, the most important predatory mite in vineyards of northern Switzerland. Entomophaga 33: 240-255. 

Boselli M.& Scannavini M. 2001. Control of grape moth in Emilia-Romagna. Informatore Agrario 57(19): 97-100. 

Boselli M., Scannavini M. & Melandri M. 2000. Comparison of control strategies against the grape moth. Informatore Agrario 56(19): 61-65. 

Camporese P. & Duso C. 1996. Different colonization patterns of phytophagous and predatory mites (Acari: Tetranychidae, Phytoseiidae) on three grape varieties: a case study. Experimental and Applied 

Acarology 20: 1-22. 

Caroli L. & Boselli M. 1998. Evaluation of efficacy of a new Bacillus thuringiensis aizawai based product against the grape moth, Lobesia botrana. Atti Giornate fitopatologiche, Scicli e Ragusa,3-7 

maggio,1998: 293-296. 

149


Daane K.M., Bentley W.J., Walton V.M. et al. 2006. New controls investigated for vine mealybug. California Agriculture 60(1): 31-38. 

Daane K.M., Cooper M.L., Triapitsyn S.V. et al. 2008. Integrated management of mealybugs in California vineyards. Acta Horticulturae 785: 235-252. 

Daane K.M. & Yokota G.Y. 1997. Release strategies affect survival and distribution of green lacewings (Neuroptera: Chrysopidae) in augmentation programs. Environmental Entomology 26: 455-464. 

Daane K.M., Yokota,G.Y., Zheng Y. & Hagen, K.S. 1996. Inundative release of common green lacewings (Neuroptera: Chrysopidae) to suppress Erythroneura variabilis and E. elegantula (Homoptera: 

Cicadellidae) in vineyards. Environmental Entomology 25: 1224-1234. 

Delbac L., Brustis J.M., Deliere L. et al. 2006. Development of decision rules for pest vineyard management. Bulletin OILB/SROP 29(11): 41. 

Dongiovanni C., Giampaolo C., di Carolo M., Natale P. & Venerito P. 2008. Evaluation of different application modes of Bacillus thuringiensis against grape moth of grapevine in Apulia. Giornate 

Fitopatologiche 2008, Cervia RA, 12-14 marzo 2008,Vol. 1: 199-202. 

Duso C., Pozzebon A. & Malagnini V. 2006. Augmentative releases of beneficials in vineyards: factors affecting predatory mite (Acari: Phytoseiidae) persistence in the long-term period. Bulletin 

OILB/SROP 29(11): 215-219. 

Duso C. & Vettorazzo E. 1999. Mite population dynamics on different grape varieties with or without phytoseiids released (Acari: Phytoseiidae). Experimental and Applied Acarology 23: 741-763. 

El Wakeil N.E., Farghaly H.T. & Ragab Z.A. 2008. Efficacy of inundative releases of Trichogramma evanescens in controlling Lobesia botrana in vineyards in Egypt. Journal of Pest Science 81: 49-55. 

English Loeb G., Villani M.,Martinson T., Forsline A. & Consolie N. 1999. Use of entomopathogenic nematodes for control of grape phylloxera (Homoptera: Phylloxeridae): a laboratory evaluation. 

Environmental Entomology 28: 890-894. 

Fretay G. du & Quenin H. 2000. Evaluation of a new formulation of Bacillus thuringiensis against European grapevine moth [Lobesia botrana] in France. Bulletin OILB/SROP 23(4): 175-177. 

Garnier Geoffroy F., Malosse C., Durier C. & Hawlitzky N. 1999. Behaviour of Trichogramma brassicae Bezdenko (Hym.: Trichogrammatidae) towards Lobesia botrana Denis & Schiffermuller (Lep.: 

Tortricidae). Annales de la Societe Entomologique de France 35(Supp.): 390-396. 

Glenn D.C. & Hoffmann A.A. 1997. Developing a commercially viable system for biological control of light brown apple moth (Lepidoptera: Tortricidae) in grapes using endemic Trichogramma 

(Hymenoptera: Trichogrammatidae). Journal of Economic Entomology 90: 370-382. 

Hera E., Tudorache M., Mincea C. & Pasareanu A. 2004. Chemical and biological control of the Hyphantria cunea Drury. in vineyard. Analele Institutului de Cercetare Dezvoltare pentru Protectia 

Plantelor, 2004, publ.2005, 33: 259-264. 

Hommay G., Gertz C.,Kienlen J.C., Pizzol J. & Chavigny P. 2002. Comparison between the control efficacy of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) and two 

Trichogramma cacoeciae Marchal strains against grapevine moth (Lobesia botrana Den. & Schiff.), depending on their release density. Biocontrol Science and Technology 12: 569-581. 

Huber L. & Kirchmair M. 2007. Evaluation of efficacy of entomopathogenic fungi against small-scale grape-damaging insects in soil - experiences with grape phylloxera. Acta Horticulturae 733: 167-171. 

Ifoulis A.A. & Savopoulou Soultani M. 2003. Biological control of Lobesia botrana (Lepidoptera: Tortricidae) larvae by using different formulations of Bacillus thuringiensis in 11 vine cultivars under 

field conditions. Journal of Economic Entomology 97: 340-343. 

Kapongo J.P., Kevan P.G. & Giliomee J.H. 2007. Control of Mediterranean fruit fly Ceratitis capitata (Diptera: Tephritidae) with the parasitoid Muscidifurax raptor (Hymenoptera: Pteromalidae) in 

vineyards. HortScience 42(6): 1400-1404. 

Keil S.& Schruft G. 1998. Effectiveness of Bacillus thuringiensis on the grape vine and grape berry moth (Lobesia botrana and Eupoecilia ambiguella). Bulletin OILB/SROP 21(2): 63-65. 

Kirchmair M., Hoffman M., Neuhauser S., Strasser H. & Huber L. 2007. Persistence of GranMetReg., a Metarhizium anisopliae based product, in grape phylloxera-infested vineyards. Bulletin OILB/SROP 

30(7): 137-142. 

Kirchmair M., Huber L., Leither E. & Strasser H. 2005. The impact of the fungal BCA Metarhizium anisopliae on soil fungi and animals. Bulletin OILB/SROP 28(2): 157-161. 

Kirchmair M., Huber L., Porten M., Rainer J. & Strasser H. 2004. Metarhizium anisopliae, a potential agent for the control of grape phylloxera. BioControl 49: 295-303. 

Laccone G. 2007. Control of the grape berry moth based on active substances. Informatore Agrario 63(26): 67-69. 

Laccone G., Scarpelli P.G., Spataro D., Caterisano R. 2004. Protecting wine grape vines in the South. Informatore Agrario 60(21): 65-70. 

Laengle T., Kirchmair M., Bauer T. et al. 2004. Environmental risk assessment of soil-applied fungal biological control agents with respect to European registration. Bulletin-OILB/SROP. 2004; 27(8): 

197-200 

Lopes R.B., Tamai M.A., Alves, S.B., Silveira-Neto S. & Salvo S. de 2002. Occurrence of thrips in Niagara table grape and their control with insecticides thiacloprid and methiocarb in association with 

Metarhizium anisopliae. Revista Brasileira de Fruticultura 24(1): 269-272. 

Maheshkumar Katke & Balikai R.A. 2008. Management of grape mealy bug, Maconellicoccus hirsutus (Green). Indian Journal of Entomology 70(3): 232-236. 

Mani M. 2008. Polyhouse efficacy of Cryptolaemus montrouzieri Mulsant for the suppression of Planococcus citri (Risso) on grapes and Ferrisia virgata (Cockerell) on guava. Journal of Insect Science 

Ludhiana 21(2): 202-204. 

Marchesini E., Ruggiero P. & Posenato G. 2006. Efficacy of Bacillus thuringensis subsp. aizawai in the control of grape berry moth (Lobesia botrana Den. & Schiff.). Giornate Fitopatologiche 2006, 

Riccione RN, 27-29 marzo 2006 Atti, vol. 1: 105-110 

150

Appendix 8 

Marshall D.B. & Lester P.J. 2001. The transfer of Typhlodromus pyri on grape leaves for biological control of Panonychus ulmi (Acari: Phytoseiidae, Tetranychidae) in vineyards in Ontario, Canada. 

Biological Control 20: 228-235. 

Mazzocchetti A., Angelucci S., Casolari A. et al. 2004. Mating disruption technique for the control of Lobesia botrana (Denis & Schiffermuller) (Tortricidae) on pergola-trained grapevines in Abruzzo. 

Giornate Fitopatologiche 2004, Montesilvano-Pescara, 4-6 maggio 2004, Atti, vol. 1: 77-82. 

Mescalchin E. 2007. Protection strategies in organic viticulture. Notiziario ERSA 2007, publ. 2008, 20(4): 59-61. 

Mitrea I., Stan C., Tuca O. 2007. Research regarding the integrate management of the vine moth (Lobesia botrana Den et Schiff.) at the Dealurile Craiovei vineyard. Bulletin of University of Agricultural 

Sciences and Veterinary Medicine Cluj Napoca Agriculture 63/64: 201-206. 

Moiraghi G., Morando A., Sozzani F. & Lembo S. 2004. Trials of grape berry moth control. Giornate Fitopatologiche 2004, Montesilvano-Pescara, 4-6 maggio 2004, Atti, vol. 1: 71-76. 

Morandi Filho W.J., Botton M., Grutzmacher A.D. & Zanardi O.Z. 2007. Effect of Bacillus thuringiensis and chemical insecticides for the control of Argyrotaenia sphaleropa (Meyrick, 1909) 

(Lepidoptera: Tortricidae) in vineyards. Arquivos do Instituto Biologico Sao Paulo 74(2): 129-134. 

Morando A., Lembo S., Marenco, G.L.,Cerrato M., Morando P. & Bevione D. 1998. Control of grape berry moth with biological preparations in comparison with insect growth regulators and 

organophosphates. Atti Giornate fitopatologiche, Scicli e Ragusa, 3-7 maggio, 1998: 201-204. 

Nagarkatti S., Tobin P.C., Saunders M.C. & Muza A.J. 2002. Role of the egg parasitoid Trichogramma minutum in biological control of the grape berry moth, Endopiza viteana. BioControl 47: 373-385. 

Nagargatti S., Tobin P.C., Saunders M.C. & Muza A.J. 2003. Release of native Trichogramma minutum to control grape berry moth. Canadian Entomologist 135: 589-598 . 

Neves M. & Frescata C. 2001. TUREX (Bacillus thuringiensis ssp. kurstaki x ssp. aizawai) for the control of Lobesia botrana third generation in Bairrada (Portugal). Bulletin OILB/SROP 24(7): 109-111. 

Pryke J.S. & Samways M.J. 2007. Current control of phytosanitary insect pests in table grape vineyards of the Hex River Valley, South Africa. African Entomology 15(1): 25-36. 

Remund U. & Bigler F. 1986. Tests for parasitism of the grape berry moth, Eupoecilia ambiguella Hubner (Lepidoptera, Tortricidae) by Trichogramma dendrolimi Mastsumura and Trichogramma maidis 

Pintureau et Voegele (Hymenoptera, Trichogrammatidae). Journal of Applied Entomology 102: 169-178. 

Roditakis N. 2003. Integrated control of grape berry moth Lobesia botrana Den. & Schiff. (Lepidoptera: Tortricidae) in Greece - present status and perspectives. Bulletin OILB/SROP 26(8): 145-146. 

Ruiz de Escudero I., Estela A., Escriche B. & Caballero P. 2007. Potential of the Bacillus thuringiensis toxin reservoir for the control of Lobesia botrana (Lepidoptera: Tortricidae), a major pest of grape 

plants. Applied and Environmental Microbiology 73: 337-340. 

Samoilov Yu K. 2003. Vineyards without chemicals. Zashchita i Karantin Rastenii 6: 22-23. 

Saunders M.C. & All J.N.1985. Association of entomophilic rhabditoid nematode populations with natural control of first-instar larvae of the grape root borer, Vitacea polistiformis, in concord grape 

vineyards. Journal of Invertebrate Pathology 45: 147-151. 

Segonca C. & Leisse N. 1989. Enhancement of the egg parasite Trichogramma semblidis (Auriv.) (Hym., Trichogrammatidae) for control of both grape vine moth species in the Ahr Valley. Journal of 

Applied Entomology 107: 41-45 

Subic M. 2007. Multi-year trials of the chemical, biotechnological and biological control of European grape vine moth (Lobesia botrana) in the Meimurje wine region. Glasilo Biljne Zastite 7(4): 245-254. 

Takahashi F., Inoue M., Takafuji A. 1998. Management of the spider-mite population in a vinyl house vinery by releasing Phytoseiulus persimilis Athias-Henriot onto the ground cover. Japanese Journal 

of Applied Entomology and Zoology 42: 71-76. 

Thomson L.J. & Hoffmann A.A. 2002. Laboratory fecundity as predictor of field success in Trichogramma carverae (Hymenoptera: Trichogrammatidae). Journal of Economic Entomology 95: 912-917. 

Tsitsipis J.A., Roditakis N., Michalopoulos G. et al. 2003. A novel scarring symptom on seedless grapes in the Corinth region (Peloponnese, southern Greece) caused by the western flower thrips, 

Frankliniella occidentalis, and pest control tests. Bulletin OILB/SROP 26(8): 259-263. 

Van Driesche R.G. & Bellows T.S. 1996. Biological Control. Chapman & Hall, New York, NY, USA, 539 pp. 

Walton V.M. & Pringle K.L. 1999. Effects of pesticides used on table grapes on the mealybug parasitoid Coccidoxenoides peregrinus (Timberlake) (Hymenoptera: Encyrtidae). South African Journal for 

Enology and Viticulture 20(1): 31-34 

Walton V.M. & Pringle K.L. 2004. Vine mealybug, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae), a key pest in South African vineyards. A review. South African Journal of Enology and 

Viticulture 25(2): 54-62. 

Williams R.N., Fickle D.S., Grewal P.S. & Meyer J.R. 2002. Assessing the potential of entomopathogenic nematodes to control the grape root borer Vitacea polistiformis (Lepidoptera: Sesiidae) through 

laboratory and greenhouse bioassays. Biocontrol Science and Technology 12: 35-42. 

Wunderlich L.R. & Giles D.K. 1999. Field assessment of adhesion and hatch of Chrysoperla eggs mechanically applied in liquid carriers. Biological-Control. 1999; 14(3): 159-167. 

Zimmermann O. 2004. Use of Trichogramma wasps in Germany: present status of research and commercial application of egg parasitoids against lepidopterous pests for crop and storage protection. 

Gesunde Pflanzen 56(6): 157-166. 

151

Appendix 9. References on classical biological control against insect pests (cited in Chapter 3) 

9.1. Biocontrol agents not precisely known 

Type of work Pest (genus level) References* 

Prospective studies (55%) (88) 

Aproaerema (89) 

Cameraria (61) 

Cryptococcus (175) (94) 

Diabrotica (154) 

Hypsipyla (141) 

Liriomyza (87) 

Lymanthria (70)(72) 

Scirtothrips (45) 

Tetranychus 

Retrospective studies (35%) (166) 

Chilo (128) 

Cinara (56) 

Cosmopolites (103) 

Maconellicoccus (47) 

mealybugs (191) 

Mononychellus (97) 

Phenacoccus 

Other studies (10%) (82) 

Pest biology Enarmonia (88) 

* Numbers correspond to refernces presented in section 9.4 

152

Appendix 9 

9.2. Details on the use of pathogens, nematodes and predators as agents of Classical Biological Control 

Pest BCA lifestyle BCA References* 

Aceria 

Fungus 

Hirsutella 

(114) 

Predatory mite Neoseiulus 

Adelges Predatory Insect Laricobius (119) 

Anticarsia Virus Nucleopolyhedrovirus (197) 

Aphids Predatory Insect Harmonia (48) (127) 

Aphis Fungus Neozygites (19) (90) (91) (137) 

Coptotermes Fungus Beauvaria & Metarhizium (168) 

Lymantria Fungus 

Microspora 

(35) 

Virus 

Nucleopolyhedrovirus 

Maconellicoccus Predatory Insect Cryptolaemus 

(165) 

Scymnus 

Mononychellus Fungus 

Neozygites 

(16) 

Predatory mite Neosiulus &Typhlodromalus 

Oryctes Virus _ (51) (86) 

Prostephanus Predatory Insect Teretrius (51) 

Review Fungus _ (14) (39) (42) (43) 

Review Nematode _ (14) (55) (124) (125) (193) (194) 

Sirex Nematode Deladenus (81) 

Solenopsis Fungus Vairimorpha (73) (169) (170) 

* Numbers correspond to refernces presented in section 9.4 

153

Ris & Malausa (Appendix for Chapter 3) 

9.3 Categorization of publications related to Insect parasitoids as ClBCA according to the type of work 

Pest Biology 

Pest rearing : (83, 183) 

BCA Biology 

BCA inventories : (30, 34, 65) (67) (88) (157) (178) 

BCA systematics: (18, 52, 123) (36) (186) 

BCA molecular characterization: (121, 132) 

BCA rearing: (21, 58, 92, 163) (171) 

BCA biology: (6, 10, 37) (74) (77) (85) (98) (100) (102) (104) (105) (158) (159) (160) (172) (190) (195) 

BCA Evaluation: (12, 44, 46) (57) (80) (108) (151) 

BCA Field Implications 

Pre-release survey: (9, 60, 66) (122) (140) (166) 

BCA introduction : see table 1 

Post-release survey : (20, 22, 32) (33) (36) (50) (54) (64) (68) (76) (78) (106) (107) (113) (109) (135) (142) (145) (146) (148) (150) (162) (179) 

Non-intended effects 

(24, 29, 38) (58) (71) (84) (92) (65) (101) (129) (149) (155) (184) (189) 

Biocontrol disruption 

(17, 27, 69) (95) (130) (147) (180) 

Miscellaneous 

Economic valuation: (23) 

Review: (75, 112, 152) (153) 

Miscellaneous: (111, 115, 116) (139) (176) 

“Conservation BC-like” : (173) 

154

Appendix 9 

References 

1. Abd-Rabou S. 2002. Biological control of two species of whiteflies by Eretmocerus siphonini (Hymenoptera: Aphelinidae) in Egypt. Acta Phytopathologica et Entomologica Hungarica 37: 

257-60 

2. Abd-Rabou S. 2004. Biological control of Bemisia tabaci biotype "B" (Homoptera : Aleyrodidae) by introduction, release and establishment of Eretmocerus hayati (Hymenoptera : 

Aphelinidae). Journal of Pest Science 77: 91-4 

3. Abd-Rabou S. 2005. Importation, colonization and establishment of Coccophagus cowperi Gir. (Hymenoptera : Aphelinidae) on Saissetia coffeae (Walk.) (Homoptera : Coccidae) in Egypt. 

Journal of Pest Science 78: 77-81 

4. Abd-Rabou S. 2006. Biological control of the leafminer, Liriomyza trifolii by introduction, releasing, evaluation of the parasitoids Diglyphus isaea and Dacnusa sibirica on vegetables crops 

in greenhouses in Egypt. Archives of Phytopathology and Plant Protection 39: 439-43 

5. Aebi A, Schonrogge K, Melika G, Quacchia A, Alma A, Stone GN. 2007. Native and introduced parasitoids attacking the invasive chestnut gall wasp Dryocosmus kuriphilus. Bulletin 

OEPP/EPPO Bulletin 37: 166-71 

6. Aldrich JR, Zhang A. 2002. Kairomone strains of Euclytia flava (Townsend), a parasitoid of stink bugs. Journal of Chemical Ecology 28: 1565-82 

7. Alleck M, Seewooruthun SI, Ramlugun D. 2006. Cypress aphid status in Mauritius & trial releases of Pauesia juniperorum (Hymenoptera: Braconidae), a promising biocontrol agent. Revue 

Agricole et Sucriere de l'Ile Maurice 85: 60-7 

8. Alvarenga CD, Brito ES, Lopes EN, Silva MA, Alves DA, et al. 2005. Introduction and recovering of the exotic parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: 

Braconidae) in commercial guava orchards in the north of the state of Minas Gerais, Brazil. Neotropical Entomology 34: 133-6 

9. Alyokhin AV, Yang PJ, Messing RH. 2001. Distribution and parasitism of Sophonia rufofascia (Homoptera: Cicadellidae) eggs in Hawaii. Annals of the Entomological Society of America 

94: 664-9 

10. Amalin DM, Pena JE, Duncan RE. 2005. Effects of host age, female parasitoid age, and host plant on parasitism of Ceratogramma etiennei (Hymenoptera: Trichogrammatidae). Florida 

Entomologist 88: 77-82 

11. Anagnou-Veroniki M, Papaioannou-Souliotis P, Karanastasi E, Giannopolitis CN. 2008. New records of plant pests and weeds in Greece, 1990-2007. Hellenic Plant Protection Journal 1: 55- 

78 

12. Andreassen LD, Kuhlmann U, Mason PG, Holliday NJ. 2007. Classical biological control of the cabbage root fly, Delia radicum, in Canadian canola: an analysis of research needs. CAB 

Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2 

13. Argov Y, Gazit Y. 2008. Biological control of the Mediterranean fruit fly in Israel: Introduction and establishment of natural enemies. Biological Control 46: 502-7 

14. Ariori SL, Dara SK. 2007. Predation of Neozygites tanajoae-infected cassava green mites by the predatory mite, Typhlodromalus aripo (Acari: Phytoseiidae). Agriculturae Conspectus 

Scientificus (Poljoprivredna Znanstvena Smotra) 72: 169-72 

15. Aristizabal ALF, Salazar EHM, Mejia MCG, Bustillo PAE. 2004. Introduction and evaluation of Phymastichus coffea (Hymenoptera: Eulophidae) in smallholder coffee farms, through 

participatory research. Revista Colombiana de Entomologia 30: 219-24 

16. Barlow ND, Caldwell NP, Kean JM, Barron MC. 2000. Modelling the use of NPV for the biological control of Asian gypsy moth Lymantria dispar invading New Zealand. Agricultural and 

Forest Entomology 2: 173-84 

17. Batchelor TP, Hardy ICW, Barrera JF, Perez-Lachaud G. 2005. Insect gladiators II: Competitive interactions within and between bethylid parasitoid species of the coffee berry borer, 

Hypothenemus hampei (Coleoptera: Scolytidae). Biological Control 33: 194-202 

18. Baur H, Muller FJ, Gibson GAP, Mason PG, Kuhlmann U. 2007. A review of the species of Mesopolobus (Chalcidoidea: Pteromalidae) associated with Ceutorhynchus (Coleoptera: 

Curculionidae) host-species of European origin. Bulletin of Entomological Research 97: 387-97 

19. Bazzocchi GG, Lanzoni A, Accinelli G, Burgio G. 2004. Overwintering, phenology and fecundity of Harmonia axyridis in comparison with native coccinellid species in Italy. BioControl 49: 

245-60 

20. Bento JMS, Moraes GJd, Matos APd, Bellotti AC. 2000. Classical biological control of the mealybug Phenacoccus herreni (Hemiptera: Pseudococcidae) in northeastern Brazil. 

Environmental Entomology 29: 355-9 

21. Berg MAvd, Greenland J. 1999. Rearing and releasing methods for Encarsia cf. smithi (Hym.: Aphelinidae), used in a classical biological control programme for the spiny blackfly, 

Aleurocanthus spiniferus (Hem.: Aleyrodidae). Neltropika Bulletin: 56-8 

22. Berg MAvd, Greenland J. 2001. Pest status of two blackfly species on citrus in South Africa and Swaziland. African Plant Protection 7: 53-7 

23. Berg MAvd, Hoppner G, Greenland J. 2000. An economic study of the biological control of the spiny blackfly, Aleurocanthus spiniferus (Hemiptera: Aleyrodidae), in a citrus orchard in 

Swaziland. Biocontrol Science and Technology 10: 27-32 

155


24. Boyd EA, Hoddle MS. 2007. Host specificity testing of Gonatocerus spp. egg-parasitoids used in a classical biological control program against Homalodisca vitripennis: a retrospective 

analysis for non-target impacts in southern California. Biological Control 43: 56-70 

25. Briano JA, Williams DF. 2002. Natural occurrence and laboratory studies of the fire ant pathogen Vairimorpha invictae (Microsporida: Burenellidae) in Argentina. Environmental 

Entomology 31: 887-94 

26. Casagrande RA, Tewksbury LA. 2005. Lily leaf beetle biological control: research report to the North American Lily Society - January 4, 2006. Lily Yearbook of the North American Lily 

Society, Inc.: 35-41 

27. Chacon JM, Landis DA, Heimpel GE. 2008. Potential for biotic interference of a classical biological control agent of the soybean aphid. Biological Control 46: 216-25 

28. Charles J. 2001. Introduction of a parasitoid for mealybug biocontrol: a case study under new environmental legislation. New Zealand Plant Protection Volume 54, 2001. Proceedings of a 

conference, Quality Hotel, Palmerston North, New Zealand, 14-16 August 2001: 37-41 

29. Charles JG, Allan DJ. 2002. An ecological perspective to host-specificity testing of biocontrol agents. New Zealand Plant Protection Volume 55, 2002. Proceedings of a conference, Centra 

Hotel, Rotorua, New Zealand, 13-15 August 2002 

30. Chinajariyawong A, Clarke AR, Jirasurat M, Kritsaneepiboon S, Lahey HA, et al. 2000. Survey of opiine parasitoids of fruit flies (Diptera: Tephritidae) in Thailand and Malaysia. Raffles 

Bulletin of Zoology 48: 71-101 

31. Conlong DE, Goebel R. 2002. Biological control of Chilo sacchariphagus (Lepidoptera: Crambidae) in Mocanbique: the first steps. Proceedings of the Annual Congress - South African 

Sugar Technologists' Association 

32. Cossentine JE, Kuhlmann U. 2007. Introductions of parasitoids to control the apple ermine moth in British Columbia. In Biological control: a global perspective, pp. 13-9 

33. Costanzi M, Frassetti F, Malausa JC. 2003. Biological control of the psyllid Ctenarytaina eucalypti Maskell in eucalyptus plantations of Ligurian Riviera. Informatore Fitopatologico 53: 52-6 

34. Coutinot D, Hoelmer K. 1999. Parasitoids of Lygus spp. in Europe and their potential for biological control of Lygus spp. in North America. Proceedings of the Fifth International 

Conference on Pests in Agriculture, Part 3, Montpellier, France, 7-9 December, 1999. 

35. Culliney TW, Grace JK. 2000. Prospects for the biological control of subterranean termites (Isoptera: Rhinotermitidae), with special reference to Coptotermes formosanus. Bulletin of 

Entomological Research 90: 9-21 

36. Daane KM, Cooper ML, Triapitsyn SV, Andrews JW, Jr., Ripa R. 2008. Parasitoids of obscure mealybug, Pseudococcus viburni (Hem.: Pseudococcidae) in California: establishment of 

Pseudaphycus flavidulus (Hym.: Encyrtidae) and discussion of related parasitoid species. Biocontrol Science and Technology 18: 43-57 

37. Daane KM, Sime KR, Wang XG, Nadel H, Johnson MW, et al. 2008. Psyttalia lounsburyi (Hymenoptera: Braconidae), potential biological control agent for the olive fruit fly in California. 

Biological Control 44: 79-89 

38. Day WH. 2005. Changes in abundance of native and introduced parasites (Hymenoptera: Braconidae), and of the target and non-target plant bug species (Hemiptera: Miridae), during two 

classical biological control programs in alfalfa. Biological Control 33: 368-74 

39. Delalibera I, Jr., Humber RA, Hajek AE. 2004. Preservation of in vitro cultures of the mite pathogenic fungus Neozygites tanajoae. Canadian Journal of Microbiology 50: 579-86 

40. Dillon AB, Rolston AN, Meade CV, Downes MJ, Griffin CT. 2008. Establishment, persistence, and introgression of entomopathogenic nematodes in a forest ecosystem. Ecological 

Applications 18: 735-47 

41. Dimitrov A, Karadjova O, Sengalevich G. 2008. Investigation on the potential of a new imported parasitoid against aphids in Bulgaria. Rasteniev'dni Nauki 45: 25-7 

42. Elliot SL, Moraes GJd, Delalibera I, Jr., Silva CADd, Tamai MA, Mumford JD. 2000. Potential of the mite-pathogenic fungus Neozygites floridana (Entomophthorales: Neozygitaceae) for 

control of the cassava green mite Mononychellus tanajoa (Acari: Tetranychidae). Bulletin of Entomological Research 90: 191-200 

43. Elliot SL, Mumford JD, Moraes GJd. 2003. The role of resting spores in the survival of the mite-pathogenic fungus Neozygites floridana from Mononychellus tanajoa during dry periods in 

Brazil. Journal of Invertebrate Pathology 81: 148-57 

44. Emana G. 2005. Suitability of Chilo partellus, Sesamia calamistis and Busseola fusca for the development of Cotesia flavipes in Ethiopia: implication for biological control. Ethiopian Journal 

of Biological Sciences 4: 123-34 

45. Fiaboe KKM, Fonseca RL, Moraes GJd, Ogol CKPO, Knapp M. 2006. Identification of priority areas in South America for exploration of natural enemies for classical biological control of 

Tetranychus evansi (Acari: Tetranychidae) in Africa. Biological Control 38: 373-9 

46. Folgarait PJ, Patrock RJW, Gilbert LE. 2006. Development of Pseudacteon nocens (Diptera: Phoridae) on Solenopsis invicta and Solenopsis richteri fire ants (Hymenoptera: Formicidae). 

Journal of Economic Entomology 99: 295-307 

47. Franco JC, Suma P, Borges da Silva E, Mendel Z. 2003. Management strategies of mealybug pests of citrus in Mediterranean countries. Bulletin OILB/SROP 26: 137 

48. Fuxa JR, Richter AR. 1999. Classical biological control in an ephemeral crop habitat with Anticarsia gemmatalis nucleopolyhedrovirus. BioControl 44: 403-19 

49. Garcia-Mari F, Vercher R, Costa-Comelles J, Marzal C, Villalba M. 2004. Establishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae) as a biological control agent for the 

citrus leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Spain. Biological Control 29: 215-26 

156

Appendix 9 

50. Gariepy TD, Kuhlmann U, Gillott C, Erlandson M. 2008. Does host plant influence parasitism and parasitoid species composition in Lygus rugulipennis? A molecular approach. Bulletin of 

Entomological Research 98: 217-21 

51. Gautam RD. 2003. Classical biological control of pink hibiscus mealy bug, Maconellicoccus hirsutus (green) in the Caribbean. Plant Protection Bulletin (Faridabad) 55: 1-8 

52. Gibson GAP, Gillespie DR, Dosdall L. 2006. The species of Chalcidoidea (Hymenoptera) introduced to North America for biological control of the cabbage seedpod weevil, and the first 

recovery of Stenomalina gracilis (Chalcidoidea: Pteromalidae). Canadian Entomologist 138: 285-91 

53. Gilbert LE, Barr CL, Calixto AA, Cook JL, Drees BM, et al. 2008. Introducing phorid fly parasitoids of red imported fire ant workers from South America to Texas: Outcomes vary by 

region and by pseudacteon species released. Southwestern Entomologist 33: 15-29 

54. Gillespie DR, Mason PG, Dosdall LM, Bouchard P, Gibson GAP. 2006. Importance of long-term research in classical biological control: an analytical review of a release against the cabbage 

seedpod weevil in North America. Journal of Applied Entomology 130: 401-9 

55. Gnanvossou D, Hanna R, Yaninek JS, Toko M. 2005. Comparative life history traits of three neotropical phytoseiid mites maintained on plant-based diets. Biological Control 35: 32-9 

56. Gold CS, Pena JE, Karamura EB. 2001. Biology and integrated pest management for the banana weevil Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae). Integrated Pest 

Management Reviews 6: 79-155 

57. Goolsby JA, DeBarro PJ, Kirk AA, Sutherst RW, Canas L, et al. 2005. Post-release evaluation of biological control of Bemisia tabaci biotype "B" in the USA and the development of 

predictive tools to guide introductions for other countries. Biological Control 32: 70-7 

58. Grandgirard J, Hoddle MS, Petit JN, Percy DM, Roderick GK, Davies N. 2007. Pre-introductory risk assessment studies of Gonatocerus ashmeadi (Hymenoptera: Mymaridae) for use as a 

classical biological control agent against Homalodisca vitripennis (Hemiptera: Cicadellidae) in the Society Islands of French Polynesia. Biocontrol Science and Technology 17: 809-22 

59. Grandgirard J, Hoddle MS, Petit JN, Roderick GK, Davies N. 2008. Engineering an invasion: classical biological control of the glassy-winged sharpshooter, Homalodisca vitripennis, by the 

egg parasitoid Gonatocerus ashmeadi in Tahiti and Moorea, French Polynesia. Biological Invasions 10: 135-48 

60. Grandgirard J, Hoddle MS, Triapitsyn SV, Petit JN, Roderick GK, Davies N. 2007. First records of Gonatocerus dolichocerus Ashmead, Palaeoneura sp., Anagrus sp. (Hymenoptera: 

Mymaridae), and Centrodora sp. (Hymenoptera: Aphelinidae) in French Polynesia, with notes on egg parasitism of the glassy-winged sharpshooter, Homalodisca vitripennis (Germar) 

(Hemiptera: Cicadellidae). Pan-Pacific Entomologist 83: 177-84 

61. Gwiazdowski RA, Driesche RGv, Desnoyers A, Lyon S, Wu S, et al. 2006. Possible geographic origin of beech scale, Cryptococcus fagisuga (Hemiptera: Eriococcidae), an invasive pest in 

North America. Biological Control 39: 9-18 

62. Hajek A, McManus M, Delalibera I. 2005. Catalogue of introductions of pathogens and nematodes for classical biological control of insect and mites, Forest Health Technology Enterprise 

Team 

63. Hajek AE, McManus ML, Delalibera Junior I. 2007. A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biological Control 41: 1-13 

64. Hanks LM, Millar JG, Paine TD, Campbell CD. 2000. Classical biological control of the Australian weevil Gonipterus scutellatus (Coleoptera: Curculionidae) in California. Environmental 

Entomology 29: 369-75 

65. Haye T, Achterberg Cv, Goulet H, Barratt BIP, Kuhlmann U. 2006. Potential for classical biological control of the potato bug Closterotomus norwegicus (Hemiptera: Miridae): description, 

parasitism and host specificity of Peristenus closterotomae sp. n. (Hymenoptera: Braconidae). Bulletin of Entomological Research 96: 421-31 

66. Hemachandra KS, Holliday NJ, Klimaszewski J, Mason PG, Kuhlmann U. 2005. Erroneous records of Aleochara bipustulata from North America: an assessment of the evidence. Canadian 


67. Hemachandra KS, Holliday NJ, Mason PG, Soroka JJ, Kuhlmann U. 2007. Comparative assessment of the parasitoid community of Delia radicum in the Canadian prairies and Europe: a 

search for classical biological control agents. Biological Control 43: 85-94 

68. Henne DC, Johnson SJ, Cronin JT. 2007. Population spread of the introduced red imported fire ant parasitoid, Pseudacteon tricuspis Borgmeier (Diptera: Phoridae), in Louisiana. Biological 

Control 42: 97-104 

69. Hill SL, Hoy MA. 2003. Interactions between the red imported fire ant Solenopsis invicta and the parasitoid Lipolexis scutellaris potentially affect classical biological control of the aphid 

Toxoptera citricida. Biological Control 27: 11-9 

70. Hoddle MS. 2005. Identifying the donor region within the home range of an invasive species: implications for classical biological control of arthropod pests. Second International Symposium 

on Biological Control of Arthropods, Davos, Switzerland, 12-16 September, 2005 

71. Hoddle MS. 2006. Historical review of control programs for Levuana iridescens (Lepidoptera: Zygaenidae) in Fiji and examination of possible extinction of this moth by Bessa remota 

(Diptera: Tachinidae). Pacific Science 60: 439-53 

72. Hoddle MS, Nakahara S, Phillips PA. 2002. Foreign exploration for Scirtothrips perseae Nakahara (Thysanoptera: Thripidae) and associated natural enemies on avocado (Persea americana 

Miller). Biological Control 24: 251-65 

157


73. Holst N, Meikle WG. 2003. Teretrius nigrescens against larger grain borer Prostephanus truncatus in African maize stores: biological control at work? Journal of Applied Ecology 40: 307-19 

74. Hougardy E, Bezemer TM, Mills NJ. 2005. Effects of host deprivation and egg expenditure on the reproductive capacity of Mastrus ridibundus, an introduced parasitoid for the biological 

control of codling moth in California. Biological Control 33: 96-106 

75. Hoy MA. 2005. Classical biological control of citrus pests in Florida and the Caribbean: interconnections and sustainability. Second International Symposium on Biological Control of 

Arthropods, Davos, Switzerland, 12-16 September, 2005: 237-53 

76. Hoy MA, Jeyaprakash A, Clarke-Harris D, Rhodes L. 2007. Molecular and field analyses of the fortuitous establishment of Lipolexis oregmae (Hymenoptera: Aphidiidae) in Jamaica as a 

natural enemy of the brown citrus aphid. Biocontrol Science and Technology 17: 473-82 

77. Hoy MA, Jeyaprakash A, Nguyen R. 2001. Long PCR is a sensitive method for detecting Liberobacter asiaticum in parasitoids undergoing risk assessment in quarantine. Biological Control 

22: 278-87 

78. Hoy MA, Singh R, Rogers ME. 2007. Citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae), and natural enemy dynamics in Central Florida during 2005. Florida Entomologist 

90: 358-69 

79. Hurley BP, Slippers B, Croft PK, Hatting HJ, Linde Mvd, et al. 2008. Factors influencing parasitism of Sirex noctilio (Hymenoptera: Siricidae) by the nematode Deladenus siricidicola 

(Nematoda: Neotylenchidae) in summer rainfall areas of South Africa. Biological Control 45: 450-9 

80. Jacas JA, Pena JE, Duncan RE, Ulmer BJ. 2008. Thermal requirements of Fidiobia dominica (Hymenoptera: Platygastridae) and Haeckeliania sperata (Hymenoptera: Trichogrammatidae), 

two exotic egg parasitoids of Diaprepes abbreviatus (Coleoptera: Curculionidae). BioControl 53: 451-60 

81. Jackson TA, Crawford AM, Glare TR. 2005. Oryctes virus - time for a new look at a useful biocontrol agent. Journal of Invertebrate Pathology 89: 91-4 

82. Jenner WH, Cossentine JE, Whistlecraft J, Kuhlmann U. 2005. Host rearing is a bottleneck for classical biological control of the cherry bark tortrix: a comparative analysis of artificial diets. 

Biocontrol Science and Technology 15: 519-25 

83. Jenner WH, Kuhlmann U, Cossentine JE, Roitberg BD. 2005. Reproductive biology and small-scale rearing of cherry bark tortrix and its candidate biological control agent. Journal of 


84. Johnson MT, Follett PA, Taylor AD, Jones VP. 2005. Impacts of biological control and invasive species on a non-target native Hawaiian insect. Oecologia 142: 529-40 

85. Joyce AL, Hanks LM, Paine TD, Millar JG. 2000. Effect of host larval size on sex ratio of progeny of Syngaster lepidus (Hymenoptera: Braconidae) attacking Phoracantha semipunctata 

(Coleoptera: Cerambycidae) and P. recurva borers on Eucalyptus camaldulensis. California Conference on Biological Control II, The Historic Mission Inn Riverside, California, USA, 11-12 

July, 2000 

86. Kairo MTK, Pollard GV, Peterkin DD, Lopez VF. 2000. Biological control of the hibiscus mealybug, Maconellicoccus hirsutus Green (Hemiptera: Pseudococcidae) in the Caribbean. 

Integrated Pest Management Reviews 5: 241-54 

87. Kenis M. 1999. Possibilities for classical biological control against forest pests through collaborative programmes between Europe and North Africa. Bulletin OILB/SROP 22: 145-50 

88. Kenis M, Cugala D. 2006. Prospects for the biological control of the groundnut leaf miner, Aproaerema modicella, in Africa. CAB Reviews: Perspectives in Agriculture, Veterinary Science, 

Nutrition and Natural Resources 1 

89. Kenis M, Tomov R, Svatos A, Schlinsog P, Vaamonde CL, et al. 2005. The horse-chestnut leaf miner in Europe - prospects and constraints for biological control. Second International 

Symposium on Biological Control of Arthropods, Davos, Switzerland, 12-16 September, 2005 

90. Koch RL, Carrillo MA, Venette RC, Cannon CA, Hutchison WD. 2004. Cold hardiness of the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Environmental Entomology 33: 

815-22 

91. Koch RL, Hutchison WD, Venette RC, Heimpel GE. 2003. Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by 

Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control 28: 265-70 

92. Krugner R, Johnson MW, Groves RL, Morse JG. 2008. Host specificity of Anagrus epos: a potential biological control agent of Homalodisca vitripennis. BioControl 53: 439-49 

93. Krull SME, Basedow T. 2005. Evaluation of the biological control of the pink wax scale Ceroplastes rubens Maskell (Hom., Coccidae) with the introduced parasitoid Anicetus beneficus Ishii 

& Yasumatsu (Hym., Encyrtidae) in the Central province of Papua New Guinea. Journal of Applied Entomology 129: 323-9 

94. Kuhlmann U, Toepfer S, Feng Z. 2005. Is classical biological control against western corn rootworm in Europe a potential sustainable management strategy? In Western corn rootworm: 

ecology and management 

95. Lacey LA, Unruh TR, Headrick HL. 2003. Interactions of two idiobiont parasitoids (Hymenoptera: Ichneumonidae) of codling moth (Lepidoptera: Tortricidae) with the entomopathogenic 

nematode Steinernema carpocapsae (Rhabditida: Steinernematidae). Journal of Invertebrate Pathology 83: 230-9 

96. Lambkin TA. 2004. Successful establishment of Encarsia ?haitiensis Dozier (Hymenoptera: Aphelinidae) in Torres Strait, Queensland, for the biological control of Aleurodicus dispersus 

Russell (Hemiptera: Aleyrodidae). Australian Entomologist 31: 83-91 

158

Appendix 9 

97. Langewald J, Neuenschwander P. 2002. Challenges in coordinating regional biological control projects in Africa: classical biological control versus augmentative biological control. 

Biocontrol News and Information 23: 101N-7N 

98. Lauziere I, Legaspi JC, Legaspi BC, Jr., Smith JW, Jr., Jones WA. 2001. Life-history studies of Lydella jalisco (Diptera: Tachinidae), a parasitoid of Eoreuma loftini (Lepidoptera: 

Pyralidae). BioControl 46: 71-90 

99. Lawson-Balagbo LM, Gondim MGC, Jr., Moraes GJd, Hanna R, Schausberger P. 2007. Refuge use by the coconut mite Aceria guerreronis: fine scale distribution and association with other 

mites under the perianth. Biological Control 43: 735-47 

100. Lim UT, Hoy MA. 2005. Biological assessment in quarantine of Semielacher petiolatus (Hymenoptera: Eulophidae) as a potential classical biological control agent of citrus leafminer, 

Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae), in Florida. Biological Control 33: 87-95 

101. Lim UT, Zappala L, Hoy MA. 2006. Pre-release evaluation of Semielacher petiolatus (Hymenoptera: Eulophidae) in quarantine for the control of citrus leafminer: host discrimination, 

relative humidity tolerance, and alternative hosts. Biological Control 36: 65-73 

102. Llacer E, Urbaneja A, Garrido A, Jacas JA. 2006. Temperature requirements may explain why the introduced parasitoid Quadrastichus citrella failed to control Phyllocnistis citrella in Spain. 

BioControl 51: 439-52 

103. Lopez VF, Kairo MTK. 2000. Old solutions to new problems: new perspectives on the sustainable management of pests through biological control. Proceedings of the 35th Annual Meeting, 

Caribbean Food Crops Society, Castries, St. Lucia, 25-31 July 1999 

104. Lu B, Tang C, Peng Z, Salle Jl, Wan F. 2008. Biological assessment in quarantine of Asecodes hispinarum Boucek (Hymenoptera: Eulophidae) as an imported biological control agent of 

Brontispa longissima (Gestro) (Coleoptera: Hispidae) in Hainan, China. Biological Control 45: 29-35 

105. Lyons DB. 1999. Phenology of the native parasitoid Sinophorus megalodontis (Hymenoptera: Ichneumonidae) relative to its introduced host, the pine false webworm (Hymenoptera: 

Pamphiliidae). Canadian Entomologist 131: 787-800 

106. Malausa JC, Giuge L, Fauvergue X. 2003. Acclimatization and spreading in France of Neodryinus typhlocybae (Ashmead) (Hymenoptera, Dryinidae) introduced to control Metcalfa pruinosa 

(Say) (Hemiptera, Flatidae). Bulletin de la Societe Entomologique de France 108: 97-102 

107. Mani M, Krishnamoorthy A. 2002. Classical biological control of the spiralling whitefly, Aleurodicus dispersus Russell - an appraisal. Insect Science and its Application 22: 263-73 

108. Mansfield S, Kriticos DJ, Potter KJB, Watson MC. 2005. Parasitism of gum leaf skeletoniser (Uraba lugens) in New Zealand. New Zealand Plant Protection, Volume 58, 2005. Proceedings 

of a conference, Wellington, New Zealand, 9-11 August 2005 

109. Matsumoto T, Itioka T, Nishida T. 2004. Is spatial density-dependent parasitism necessary for successful biological control? Testing a stable host-parasitoid system. Entomologia 

Experimentalis et Applicata 110: 191-200 

110. McNeill MR, Goldson SL, Proffitt JR, Phillips CB, Addison PJ. 2002. A description of the commercial rearing and distribution of Microctonus hyperodae (Hymenoptera: Braconidae) for 

biological control of Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). Biological Control 24: 167-75 

111. Messing RH. 2003. The role of parasitoids in eradication or area-wide control of tephritid fruit flies in the Hawaiian Islands. Turning the tide: the eradication of invasive species: Proceedings 

of the International Conference on eradication of island invasives 

112. Michaud JP. 2002. Classical biological control: a critical review of recent programs against citrus pests in Florida. Annals of the Entomological Society of America 95: 531-40 

113. Mills N. 2005. Classical biological control of codling moth: the California experience. Second International Symposium on Biological Control of Arthropods, Davos, Switzerland, 12-16 

September, 2005 

114. Moore D. 2002. Non-chemical control of Aceria guerreronis on coconuts. Proceedings of the International Workshop on Coconut mite (Aceria guerreronis), Coconut Research Institute, Sri 

Lanka, 6-8 January 2000 

115. Morozov AS, Rytova SV, Thompson LC. 2003. Introducing entomophagous insects to control pests: prediction of target species density. Russian Entomological Journal 12: 441-5 

116. Morozov AS, Rytova SV, Thompson LC. 2004. Introducing entomophagous insects to control pests: prediction of target species density. Russian Entomological Journal 13: 441-5 

117. Muniappan R, Meyerdirk DE, Sengebau FM, Berringer DD, Reddy GVP. 2006. Classical biological control of the papaya mealybug, Paracoccus marginatus (Hemiptera: Pseudococcidae) in 

the Republic of Palau. Florida Entomologist 89: 212-7 

118. Murguido Morales CA, Elizondo Silva AI, Moreno Rodriguez D, Caballero Figueroa S, Armas Garcia JLd. 2008. Liberation of the wasp from Costa de Marfil Cephalonomia stephanoderis 

Betrem (Hymenoptera: Bethylidae) in two locations of Guamuhaya Mountains, Cuba. Fitosanidad 12: 83-7 

119. Negloh K, Hanna R, Schausberger P. 2008. Comparative demography and diet breadth of Brazilian and African populations of the predatory mite Neoseiulus baraki, a candidate for 

biological control of coconut mite. Biological Control 46: 523-31 

120. Nijhof BW, Oudman L, Torres R, Garrido C. 2000. The introduction of Encarsia guadeloupae (Hymenoptera, Aphelinidae) for control of Aleurodicus dispersus and Lecanoideus floccissimus 

(Homoptera, Aleyrodidae) on tenerife. Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society 11: 41-7 

159


121. Niyibigira EI. 2003. Genetic variability in Cotesia flavipes and its importance in biological control of lepidopteran stemborers. In Genetic variability in /i Cotesia flavipes/ and its importance 

in biological control of lepidopteran stemborers 

122. Niyibigira EI, Abdallah ZS, Overholt WA, Lada VY, Huis Av. 2001. Distribution and abundance, in maize and sorghum, of lepidopteran stemborers and associated indigenous parasitoids in 

Zanzibar. Insect Science and its Application 21: 335-46 

123. Niyibigira EI, Overholt WA, Stouthamer R. 2004. Cotesia flavipes Cameron (Hymenoptera: Braconidae) does not exhibit complementary sex determination (ii) evidence from laboratory 

experiments. Applied Entomology and Zoology 39 

124. Onzo A, Hanna R, Janssen A, Sabelis MW. 2004. Interactions between two neotropical phytoseiid predators on cassava plants and consequences for biological control of a shared spider mite 

prey: a screenhouse evaluation. Biocontrol Science and Technology 14: 63-76 

125. Onzo A, Hanna R, Sabelis MW. 2005. Biological control of cassava green mites in Africa: impact of the predatory mite Typhlodromalus aripo. Entomologische Berichten 65: 2-7 

126. Paiva PEB, Gravena S, Amorim LCdS. 2000. Introduction of the parasitoid Ageniaspis citricola Logvinoskaya for the biological control of the citrus leafminer Phyllocnistis citrella Stainton 

in Brazil. Laranja 21: 289-94 

127. Peng F, Fuxa JR, Richter AR, Johnson SJ. 1999. Effects of heat-sensitive agents, soil type, moisture, and leaf surface on persistence of Anticarsia gemmatalis (Lepidoptera: Noctuidae) 

nucleopolyhedrovirus. Environmental Entomology 28: 330-8 

128. Penteado SdRC, Iede ET, Reis Filho W. 2000. The occurrence, distribution, damage and control of aphids of the genus Cinara on Pinus spp. in Brazil. Floresta 30: 55-64 

129. Persad AB, Hoy MA. 2003. Intra- and interspecific interactions between Lysiphlebus testaceipes and Lipolexis scutellaris (Hymenoptera: Aphidiidae) reared on Toxoptera citricidus 

(Homoptera: Aphididae). Journal of Economic Entomology 96: 564-9 

130. Persad AB, Hoy MA. 2004. Predation by Solenopsis invicta and Blattella asahinai on Toxoptera citricida parasitized by Lysiphlebus testaceipes and Lipolexis oregmae on citrus in Florida. 


131. Persad AB, Hoy MA, Nguyen R. 2007. Establishment of Lipolexis oregmae (Hymenoptera: Aphidiidae) in a classical biological control program directed against the brown citrus aphid 

(Homoptera: Aphididae) in Florida. Florida Entomologist 90: 204-13 

132. Persad AB, Jeyaprakash A, Hoy MA. 2004. High-fidelity PCR assay discriminates between immature Lipolexis oregmae and Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) within their 

aphid hosts. Florida Entomologist 87: 18-24 

133. Petit JN, Hoddle MS, Grandgirard J, Roderick GK, Davies N. 2008. Short-distance dispersal behavior and establishment of the parasitoid Gonatocerus ashmeadi (Hymenoptera: Mymaridae) 

in Tahiti: implications for its use as a biological control agent against Homalodisca vitripennis (Hemiptera: Cicadellidae). Biological Control 45: 344-52 

134. Phillips CB, Baird DB, Iline II, McNeill MR, Proffitt JR, et al. 2008. East meets west: adaptive evolution of an insect introduced for biological control. Journal of Applied Ecology 45: 948- 

56 

135. Pickett CH, Pitcairn MJ. 1999. Classical biological control of ash whitefly: factors contributing to its success in California. BioControl 44: 143-58 

136. Pina T, Verdu MJ. 2007. Establishment and dispersal of Aphytis melinus and A. lingnanensis (Hym.: Aphelinidae), two parasitoids introduced to control Chrysomphalus dictyospermi 

Morgan and Aonidiella aurantii (Maskell) (Hem.: Diaspididae) in citrus of the Valencian region (Spain). Boletin de Sanidad Vegetal Plagas 33: 311-20 

137. Poutsma J, Loomans AJM, Aukema B, Heijerman T. 2008. Predicting the potential geographical distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX model. 

BioControl 53: 103-25 

138. Protasov A, Blumberg D, Brand D, Salle Jl, Mendel Z. 2007. Biological control of the eucalyptus gall wasp Ophelimus maskelli (Ashmead): taxonomy and biology of the parasitoid species 

Closterocerus chamaeleon (Girault), with information on its establishment in Israel. Biological Control 42: 196-206 

139. Quilici S, Duyck PF, Rousse P, Gourdon F, Simiand C, Franck A. 2005. Bactrocera zonata in La Reunion island. Phytoma 

140. Ramani S, Poorani J, Bhumannavar BS. 2002. Spiralling whitefly, Aleurodicus dispersus, in India. Biocontrol News and Information 23: 55N-62N 

141. Rauf A, Shepard BM, Johnson MW. 2000. Leafminers in vegetables, ornamental plants and weeds in Indonesia: surveys of host crops, species composition and parasitoids. International 

Journal of Pest Management 46: 257-66 

142. Rizqi A, Nia M, Abbassi M, Rochd A. 2003. Establishment of exotic parasites of citrus leaf miner, Phyllocnistis citrella, in citrus groves in Morocco. Bulletin OILB/SROP 26: 1-6 

143. Rizzo MC, Verde Gl, Rizzo R, Buccellato V, Caleca V. 2006. Introduction of Closterocerus sp. in Sicily for biological control of Ophelimus maskelli Ashmead (Hymenoptera Eulophidae) 

invasive gall inducer on eucalypt trees. Bollettino di Zoologia Agraria e di Bachicoltura 38: 237-48 

144. Rodriguez A, F., Saiz G, F. 2006. Parasitoidism of Psyllaephagus pilosus Noyes (Hym.: Encyrtidae) on the blue gum psyllid, Ctenarytaina eucalypti (Maskell) (Hem.: Psyllidae) in V region 

eucalypts plantations. Agricultura Tecnica 66: 342-51 

145. Roltsch WJ. 2000. Establishment of silverleaf whitefly parasitoids in Imperial Valley. California Conference on Biological Control II, The Historic Mission Inn Riverside, California, USA, 

11-12 July, 2000 

160

Appendix 9 

146. Roltsch WJ, Meyerdirk DE, Warkentin R, Andress ER, Carrera K. 2006. Classical biological control of the pink hibiscus mealybug, Maconellicoccus hirsutus (Green), in southern California. 


147. Rossbach A, Lohr B, Vidal S. 2008. Interspecific competition between Diadegma semiclausum Hellen and Diadegma mollipla (Holmgren), parasitoids of the diamondback moth, Plutella 

xylostella (L), feeding on a new host plant. Bulletin of Entomological Research 98: 135-43 

148. Rossi MN, Fowler HG. 2003. Temporal patterns of parasitism in Diatraea saccharalis Fabr. (Lep., Crambidae) populations at different spatial scales in sugarcane fields in Brazil. Journal of 


149. Rossi MN, Fowler HG. 2004. Spatial and temporal population interactions between the parasitoids Cotesia flavipes and Tachinidae flies: considerations on the adverse effects of biological 

control practice. Journal of Applied Entomology 128: 112-9 

150. Rossi MN, Fowler HG. 2004. Spatial pattern of parasitism in Diatraea saccharalis Fab. (Lep., Crambidae) populations at two different spatial scales in sugarcane fields in Brazil. Journal of 


151. Rousse P, Gourdon F, Quilici S. 2006. Host specificity of the egg pupal parasitoid Fopius arisanus (Hymenoptera: Braconidae) in La Reunion. Biological Control 37: 284-90 

152. Rousse P, Harris EJ, Quilici S. 2005. Fopius arisanus, an egg-pupal parasitoid of Tephritidae. Overview. Biocontrol News and Information 26: 59N-69N 

153. Sands D, Liebregts W. 2005. Biological control of fruit piercing moth (Eudocima fullonia Clerck ) (Lepidoptera: Noctuidae) in the Pacific: exploration, specificity, and evaluation of 

parasitoids. Second International Symposium on Biological Control of Arthropods, Davos, Switzerland, 12-16 September, 2005 

154. Sands DPA, Murphy ST. 2001. Prospects for biological control of Hypsipyla spp. with insect agents. Hypsipyla shoot borers in Meliaceae. Proceedings of an International Workshop held at 

Kandy, Sri Lanka, 20-23 August 1996 

155. Schellhorn NA, Kuhman TR, Olson AC, Ives AR. 2002. Competition between native and introduced parasitoids of aphids: nontarget effects and biological control. Ecology 83: 2745-57 

156. Shah PA, Pell JK. 2003. Entomopathogenic fungi as biological control agents. Applied Microbiology and Biotechnology 61: 413-23 

157. Silva RGd, Silva EBd, Franco JC. 2006. Parasitoid complex of citrus leafminer on lemon orchards in Portugal. Bulletin OILB/SROP 29: 197-204 

158. Sime KR, Daane KM, Kirk A, Andrews JW, Johnson MW, Messing RH. 2007. Psyttalia ponerophaga (Hymenoptera: Braconidae) as a potential biological control agent of olive fruit fly 

Bactrocera oleae (Diptera: Tephritidae) in California. Bulletin of Entomological Research 97: 233-42 

159. Sime KR, Daane KM, Nadel H, Funk CS, Messing RH, et al. 2006. Diachasmimorpha longicaudata and D. kraussii (Hymenoptera: Braconidae), potential parasitoids of the olive fruit fly. 

Biocontrol Science and Technology 16: 169-79 

160. Singh R, Hoy MA. 2007. Tools for evaluating Lipolexis oregmae (Hymenoptera: Aphidiidae) in the field: effects of host aphid and host plant on mummy location and color plus improved 

methods for obtaining adults. Florida Entomologist 90: 214-22 

161. Siscaro G, Barbagallo S, Longo S, Reina P, Zappala L. 1999. Results of the introduction of exotic parasitoids of Phyllocnistis citrella Stainton (Lepidoptera, Gracillariidae) in Sicily. 

Phytophaga (Palermo) 9: 31-9 

162. Siscaro G, Caleca V, Reina P, Rizzo MC, Zappala L. 2003. Current status of the biological control of the citrus leafminer in Sicily. Bulletin OILB/SROP 26: 29-36 

163. Skelley LH, Hoy MA. 2004. A synchronous rearing method for the Asian citrus psyllid and its parasitoids in quarantine. Biological Control 29: 14-23 

164. Smith D, Papacek D, Neale C. 2004. The successful introduction to Australia of Diversinervus sp. near Stramineus Compere (Hymenoptera: Encyrtidae), Kenyan parasitoid of green coffee 

scale. General and Applied Entomology 33: 33-9 

165. Solter LF, Maddox JV. 1999. Strategies for evaluating the host specificity of lepidopteran microsporidian. Revista de la Sociedad Entomologica Argentina 58: 9-16 

166. Songa JM, Overholt WA, Okello RO, Mueke JM. 2002. Control of lepidopteran stemborers in maize by indigenous parasitoids in semi-arid areas of Eastern Kenya. Biological Agriculture & 

Horticulture 20: 77-90 

167. Sosa-Gomez DR. 1999. Current status of the microbial control of agricultural pests with entomopathogenic fungi. Revista de la Sociedad Entomologica Argentina 58: 295-300 

168. Steinkraus DC, Boys GO, Rosenheim JA. 2002. Classical biological control of Aphis gossypii (Homoptera: Aphididae) with Neozygites fresenii (Entomophthorales: Neozygitaceae) in 

California cotton. Biological Control 25: 297-304 

169. Stewart-Jones A, Hodges RJ, Farman DI, Hall DR. 2006. Solvent extraction of cues in the dust and frass of Prostephanus truncatus and analysis of behavioural mechanisms leading to 

arrestment of the predator Teretrius nigrescens. Physiological Entomology 31: 63-72 

170. Stewart-Jones A, Hodges RJ, Farman DI, Hall DR. 2007. Prey-specific contact kairomones exploited by adult and larval Teretrius nigrescens: a behavioural comparison across different 

stored-product pests and different pest substrates. Journal of Stored Products Research 43: 265-75 

171. Suazo A, Arismendi N, Frank JH, Cave RD. 2006. Method for continuously rearing Lixadmontia franki (Diptera: Tachinidae), a potential biological control agent of Metamasius callizona 

(Coleoptera: Dryophthoridae). Florida Entomologist 89: 348-53 

172. Sullivan DJ, Daane KM, Sime KR, Andrews JW, Jr. 2006. Protective mechanisms for pupae of Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae), a parasitoid of the red-gum lerp 

psyllid, Glycaspis brimblecombei Moore (Hemiptera: Psylloidea). Australian Journal of Entomology 45: 101-5 

161


173. Takagi M, Okumura M, Shoubu M, Shiraishi A, Ueno T. 2005. Classical biological control of the alfalfa weevil in Japan. Second International Symposium on Biological Control of 

Arthropods, Davos, Switzerland, 12-16 September, 2005 

174. Tewksbury L, Gold MS, Casagrande RA, Kenis M. 2005. Establishment in North America of Tetrastichus setifer Thomson (Hymenoptera: Eulophidae), a parasitoid of Lilioceris lilii 

(Coleopetera: Chrysomelidae). Second International Symposium on Biological Control of Arthropods, Davos, Switzerland, 12-16 September, 2005 

175. Toepfer S, Kuhlmann U. 2004. Survey for natural enemies of the invasive alien chrysomelid, Diabrotica virgifera virgifera, in Central Europe. BioControl 49 

176. Toepfer S, Zhang F, Kiss J, Kuhlmann U. 2005. The invasion of the western corn rootworm, Diabrotica vergifera virgifera, in Europe and potential for classical biological control. Second 

International Symposium on Biological Control of Arthropods, Davos, Switzerland, 12-16 September, 2005 

177. Tribe GD, Cillie JJ. 2004. The spread of Sirex noctilio Fabricius (Hymenoptera : Siricidae) in South African pine plantations and the introduction and establishment of its biological control 

agents. African Entomology 12: 9-17 

178. Trjapitzin VA, Triapitsyn SV. 2002. A new species of Neoplatycerus (Hymenoptera: Encyrtidae) from Egypt, parasitoid of the vine mealybug, Planococcus ficus (Homoptera: 

Pseudococcidae). Entomological News 113: 203-10 

179. Tuda M, Matsumoto T, Itioka T, Ishida N, Takanashi M, et al. 2006. Climatic and intertrophic effects detected in 10-year population dynamics of biological control of the arrowhead scale by 

two parasitoids in southwestern Japan. Population Ecology 48: 59-70 

180. Urbaneja A, Llacer E, Garrido A, Jacas JA. 2003. Interspecific competition between two ectoparasitoids of Phyllocnistis citrella (Lepidoptera: Gracillariidae): Cirrospilus brevis and the 

exotic Quadrastichus sp. (Hymenoptera: Eulophidae). Biological Control 28: 243-50 

181. Vargas RI, Leblanc L, Putoa R, Eitam A. 2007. Impact of introduction of Bactrocera dorsalis (Diptera : Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera 

: Braconidae) on economically important fruit flies in French Polynesia. Journal of Economic Entomology 100: 670-9 

182. Vazquez RJ, Porter SD, Briano JA. 2006. Field release and establishment of the decapitating fly Pseudacteon curvatus on red imported fire ants in Florida. BioControl 51: 207-16 

183. Virla EG, Cangemi L, Logarzo GA. 2007. Suitability of different host plants for nymphs of the sharpshooter Tapajosa rubromarginata (Hemiptera: Cicadellidae: Proconinii). Florida 


184. Wang XG, Messing RH. 2002. Newly imported larval parasitoids pose minimal competitive risk to extant egg-larval parasitoid of tephritid fruit flies in Hawaii. Bulletin of Entomological 

Research 92: 158-63 

185. Wang Z, Huang J, Liang Z, Lian B, Lin Q, Zhong J. 2004. Introduction and application of Coccobius azumai Tachikawa (Hymenoptera: Aphelinidae). Journal of Fujian Agriculture and 

Forestry University (Natural Science Edition) 33: 313-7 

186. Wharton RA, Lopez-Martinez V. 2000. A new species of Triaspis Haliday (Hymenoptera: Braconidae) parasitic on the pepper weevil, Anthonomus eugenii Cano (Coleoptera: 

Curculionidae). Proceedings of the Entomological Society of Washington 102: 794-801 

187. White GL, Kairo MTK, Lopez V. 2005. Classical biological control of the citrus blackfly Aleurocanthus woglumi by Amitus hesperidum in Trinidad. BioControl 50: 751-9 

188. White WH, Reagan TE, Smith JW, Salazar JA. 2004. Refuge releases of Cotesia flavipes (Hymenoptera : braconidae) into the Louisiana sugarcane ecosystem. Environmental Entomology 

33: 627-32 

189. Wyckhuys KAG, Koch RL, Heimpel GE. 2007. Physical and ant-mediated refuges from parasitism: implications for non-target effects in biological control. Biological Control 40: 306-13 

190. Wyckhuys KAG, Strange-George JE, Kulhanek CA, Wackers FL, Heimpel GE. 2008. Sugar feeding by the aphid parasitoid Binodoxys communis: how does honeydew compare with other 

sugar sources? Journal of Insect Physiology 54: 481-91 

191. Yaninek S, Hanna R. 2002. Cassava green mite in Africa - a unique example of successful classical biological control of a mite pest on a Continental scale. In Biological control in IPM 

systems in Africa 

192. Zaia G, Willink E, Gastaminza G, Salas H, Villagran ME, et al. 2006. Classical biological control of the citrus leaf miner: balance realized in EEAOC. Avance Agroindustrial 27: 29-34 

193. Zannou ID, Hanna R, Agboton B, Moraes GJd, Kreiter S, et al. 2007. Native phytoseiid mites as indicators of non-target effects of the introduction of Typhlodromalus aripo for the biological 

control of cassava green mite in Africa. Biological Control 41: 190-8 

194. Zannou ID, Hanna R, Moraes GJd, Kreiter S, Phiri G, Jone A. 2005. Mites of cassava (Manihot esculenta Crantz) habitats in Southern Africa. International Journal of Acarology 31: 149-64 

195. Zhang F, Toepfer S, Riley K, Kuhlmann U. 2004. Reproductive biology of Celatoria compressa (Diptera: Tachinidae), a parasitoid of Diabrotica virgifera virgifera (Coleoptera: 

Chrysomelidae). Biocontrol Science and Technology 14: 5-16 

196. Zilahi-Balogh GMG, Kok LT, Salom SM. 2002. Host specificity of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a potential biological control agent of the hemlock wooly adelgid, 

Adelges tsugae Annand (Homoptera: Adelgidae). Biological Control 24: 192-8 

197. Zilahi-Balogh GMG, Kok LT, Salom SM. 2005. A predator case history: Laricobius nigrinus, a derodontid beetle introduced against the hemlock woolly adelgid. Second International 

Symposium on Biological Control of Arthropods, Davos, Switzerland, 12-16 September, 2005 

162

Appendix 10. Substances included in the "EU Pesticides Database" as of April 21 2009 

Substance 

Cipac 

& incl 

2008/ 

127 √ 

Category 

List 

(*) 

Inclusion 

Date 

Expiry 

Date 

Legislation 

Botanical Extract from tea tree RE A 4 01/09/2009 31/08/2019 2008/127 

Botanical Garlic extract RE A 4 01/09/2009 31/08/2019 2008/127 

Botanical Gibberellic acid '307 PG A 4 01/09/2009 31/08/2019 2008/127 

Botanical Gibberellin PG A 4 01/09/2009 31/08/2019 2008/127 

Botanical Laminarin EL C 01/04/2005 31/03/2015 05/3/EC 

Botanical Pepper RE A 4 01/09/2009 31/08/2019 2008/127 

Botanical Plant oils / Citronella oil HB A 4 01/09/2009 31/08/2019 2008/127 

Botanical Plant oils / Clove oil RE A 4 01/09/2009 31/08/2019 2008/127 

Botanical Plant oils / Rape seed oil IN, AC A 4 01/09/2009 31/08/2019 2008/127 

Botanical Plant oils / Spearmint oil PG A 4 01/09/2009 31/08/2019 2008/127 

Botanical Sea-algae extract (formerly seaalgae 

extract and seaweeds) 

PG A 4 01/09/2009 31/08/2019 2008/127 

Botanical 

copied by 

synthesis 

Botanical 

copied by 

synthesis 

Botanical 

but excluded 

Carvone PG C 01/08/2008 31/07/2018 2008/44/EC 

Ethylene PG A 4 01/09/2009 31/08/2019 2008/127 

Pyrethrins '32 IN A 4 01/09/2009 31/08/2019 2008/127 

Chemical 2,4-D '1 HB, PG A 1 01/10/2002 30/09/2012 01/103/EC 

Chemical 2,4-DB '83 HB A 1 01/01/2004 31/12/2013 03/31/EC 

Chemical 1-Methyl-cyclopropene PG C 01/04/2006 31/03/2016 06/19/EC 

Chemical Acetamiprid IN C 01/01/2005 31/12/2014 04/99/EC 

Chemical Acibenzolar-S-methyl 

(benzothiadiazole) 

PA C 01/11/2001 31/10/2011 01/87/EC 

Chemical Aclonifen '498 HB A 3 01/08/2009 31/07/2019 2008/116 

Chemical Alpha-Cypermethrin (aka 

'454 IN A 1 01/03/2005 28/02/2015 04/58/EC 

alphamethrin) 

Chemical Aluminium ammonium sulfate RE A 4 01/09/2009 31/08/2019 2008/127 

Chemical Aluminium phosphide '227 IN, RO A 3 01/09/2009 31/08/2019 2008/125 

Chemical Amidosulfuron '515 HB A 3 01/01/2009 31/12/2018 2008/40 

Chemical Amitrole (aminotriazole) '90 HB A 1 01/01/2002 31/12/2012 01/21/EC 

Chemical Azimsulfuron HB C 01/10/1999 01/10/2019 99/80/EC 

Chemical Azoxystrobin FU C 01/07/1998 01/07/2008 98/47/EC 

Chemical Beflubutamid HB C 01/12/2007 30/11/2017 07/50/EC 

Chemical Benalaxyl '416 FU A 1 01/03/2005 28/02/2015 04/58/EC 

Chemical Benfluralin '285 HB A 3 01/01/2009 31/12/2018 2008/108 

Chemical Bensulfuron '502 HB A 3 01/11/2009 31/10/2019 2009/11 

Chemical Bentazone '366 HB A 1 01/08/2001 31/07/2011 00/68/EC 

Chemical Benthiavalicarb FU C 01/08/2008 31/07/2018 08/44/EC 

Chemical Beta-Cyfluthrin '482 IN A 1 01/01/2004 31/12/2013 03/31/EC 

Chemical Bifenazate AC C 01/12/2005 30/11/2015 05/58/EC 

Chemical Bifenox '413 HB A 3 01/01/2009 31/12/2018 2008/66 

Chemical Bordeaux mixture FU A 3 01/11/2009 30/11/2016 SCoFCAH 

voted 

01.2009 

Chemical Boscalid FU C 01/08/2008 31/07/2018 08/44/EC 

Chemical Bromoxynil '87 HB A 1 01/03/2005 28/02/2015 04/58/EC 

163

Heilig et al (Appendix for Chapter 4) 

Chemical Calcium carbide RE A 4 01/09/2009 31/08/2019 2008/127 

Chemical Calcium phosphide '505 RO A 3 01/09/2009 31/08/2019 2008/125 

Chemical Captan '40 FU A 2 01/10/2007 30/09/2017 07/5/EC 

Chemical Carbendazim '263 FU A 1 01/01/2007 31/12/2009 06/135/EC 

Chemical Carfentrazone-ethyl HB C 01/10/2003 30/09/2013 03/68/EC 

Chemical Chloridazon (aka pyrazone) '111 HB A 3 01/01/2009 31/12/2018 2008/41 

Chemical Chlormequat (chloride) '143 PG A 3 01/12/2009 30/11/2019 

Chemical Chlorothalonil '288 FU A 1 01/03/2006 28/02/2016 05/53/EC 

Chemical Chlorotoluron '217 HB A 1 01/03/2006 28/02/2016 05/53/EC 

Chemical Chlorpropham '43 PG, HB A 1 01/02/2005 31/01/2015 04/20/EC 

Chemical Chlorpyrifos '221 IN, AC A 1 01/07/2006 30/06/2016 05/72/EC 

Chemical Chlorpyrifos-methyl '486 IN, AC A 1 01/07/2006 30/06/2016 05/72/EC 

Chemical Chlorsulfuron '391 HB A 3 01/09/2009 31/08/2019 

Chemical Cinidon ethyl HB C 01/10/2002 30/09/2012 02/64/EC 

Chemical Clodinafop HB A 2 01/02/2007 31/01/2017 06/39/EC 

Chemical Clofentezine '418 AC A 3 01/01/2009 31/12/2018 2008/69 

Chemical Clomazone '509 HB A 3 01/11/2008 01/11/2018 2007/76 

Chemical Clopyralid '455 HB A 2 01/01/2007 30/04/2017 06/64/EC 

Chemical Clothianidin IN C 01/08/2006 31/07/2016 06/41/EC 

Chemical Copper compounds FU A 3 01/11/2009 30/11/2016 SCoFCAH 

voted 

01.2009 

Chemical Copper hydroxide FU A 3 01/11/2009 30/11/2016 SCoFCAH 

voted 

01.2009 

Chemical Copper oxychloride FU A 3 01/11/2009 30/11/2016 SCoFCAH 

voted 

01.2009 

Chemical Cuprous oxide FU A 3 01/11/2009 30/11/2016 SCoFCAH 

voted 

01.2009 

Chemical Cyazofamid FU C 01/07/2003 30/06/2013 03/23/EC 

Chemical Cyclanilide PG C 01/11/2001 31/10/2011 01/87/EC 

Chemical Cyfluthrin '385 IN, AC A 1 01/01/2004 31/12/2013 03/31/EC 

Chemical Cyhalofop-butyl HB C 01/10/2002 30/09/2012 02/64/EC 

Chemical Cymoxanil '419 FU A 3 01/09/2009 31/08/2019 2008/125 

Chemical Cypermethrin '332 IN, AC A 1 01/03/2006 28/02/2016 05/53/EC 

Chemical Cyprodinil '511 FU A 2 01/05/2007 30/04/2017 06/64/EC 

Chemical Cyromazine '420 IN A 3 01/01/2010 31/08/2019 

Chemical Daminozide '330 PG A 1 01/03/2006 28/02/2016 05/53/EC 

Chemical Deltamethrin '333 IN A 1 01/11/2003 31/10/2013 03/5/EC 

Chemical Desmedipham '477 HB A 1 01/11/2003 31/10/2013 04/58/EC 

Chemical Dicamba '85 HB A 3 01/01/2009 31/12/2018 2008/69 

Chemical Dichlorobenzoic acid methylester FU, PGR A 3 01/09/2009 31/08/2019 2008/125 

Chemical Dichlorprop-P '476 HB A 2 01/06/2007 31/05/2017 06/74/EC 

Chemical Didecyldimethylammonium 

FU A 4 

chloride 

Chemical Difenacoum '514 RO A 4 

Chemical Difenoconazole '687 FU A 3 01/01/2009 31/12/2018 2008/69 

Chemical Diflubenzuron '339 IN A 3 01/01/2009 31/12/2018 2008/69 

Chemical Diflufenican '462 HB A 3 01/01/2009 31/12/2018 2008/66 

Chemical Dimethachlor HB A 3 01/01/2010 31/08/2019 

Chemical Dimethenamid ? P HB C 01/01/2004 31/12/2013 03/84/EC 

Chemical Dimethoate '59 IN, AC A 2 01/10/2007 30/09/2017 07/25/EC 

Chemical Dimethomorph '483 FU A 2 01/10/2007 30/09/2017 07/25/EC 

164

Appendix 10 

Chemical Dimoxystrobin FU C 01/10/2006 30/09/2016 06/75/EC 

Chemical Dinocap '98 FU, AC A 1 01/01/2007 31/12/2009 06/136/EC 

Chemical Diquat (dibromide) '55 HB A 1 01/01/2002 31/12/2011 01/21/EC 

Chemical Diuron '100 HB A 2 01/10/2008 30/09/2018 08/91/EC 

Chemical Dodemorph '300 FU A 3 01/09/2009 31/08/2019 2008/125 

Chemical Epoxiconazole '609 FU A 3 01/01/2009 31/12/2018 2008/107 

Chemical Esfenvalerate '481 IN A 1 01/08/2001 31/07/2011 00/67/EC 

Chemical Ethephon '373 PG A 2 01/08/2007 31/07/2017 06/85/EC 

Chemical Ethofumesate '233 HB A 1 01/03/2003 28/02/2013 02/37/EC 

Chemical Ethoprophos '218 NE, IN A 2 01/10/2007 30/09/2017 07/52/EC 

Chemical Ethoxysulfuron HB C 01/07/2003 30/06/2013 03/23/EC 

Chemical Etofenprox '471 IN A 3 01/01/2010 31/12/2019 

Chemical Etoxazole IN C 01/06/2005 31/05/2015 05/34/EC 

Chemical Famoxadone FU C 01/10/2002 30/09/2012 02/64/EC 

Chemical Fenamidone FU C 01/10/2003 30/09/2013 03/68/EC 

Chemical Fenamiphos (aka phenamiphos) NE A 2 01/08/2007 31/07/2017 06/85/EC 

Chemical Fenhexamid FU C 01/06/2001 31/05/2011 01/28/EC 

Chemical Fenoxaprop-P '484 HB A 3 01/01/2009 31/12/2018 2008/66 

Chemical Fenpropidin '520 FU A 3 01/01/2009 31/12/2018 2008/66 

Chemical Fenpropimorph '427 FU A 3 01/01/2009 31/12/2018 2008/107 

Chemical Fenpyroximate AC A 3 01/01/2009 31/12/2018 2008/107 

Chemical Fipronil '581 IN A 2 01/10/2007 30/09/2017 07/52/EC 

Chemical Flazasulfuron HB C 01/06/2004 31/05/2014 04/30/EC 

Chemical Florasulam HB C 01/10/2002 30/09/2012 02/64/EC 

Chemical Fluazinam '521 FU A 3 01/01/2009 31/12/2018 2008/108 

Chemical Fludioxonil '522 FU A 3 01/11/2008 01/11/2018 2007/76 

Chemical Flufenacet (formerly fluthiamide) HB C 01/01/2004 31/12/2013 03/84/EC 

Chemical Flumioxazin HB C 01/01/2003 31/12/2012 02/81/EC 

Chemical Fluoxastrobin FU C 01/08/2008 31/07/2018 08/44/EC 

Chemical Flupyrsulfuron methyl HB C 01/07/2001 30/06/2011 01/49/EC 

Chemical Fluroxypyr '431 HB A 1 01/12/2000 30/11/2010 00/10/EC 

Chemical Flurtamone HB C 01/01/2004 31/12/2013 03/84/EC 

Chemical Flusilazole '435 FU A 1 01/01/2007 30/06/2008 06/133/EC 

Chemical Flutolanil '524 FU A 3 01/01/2009 31/12/2018 2008/108 

Chemical Folpet '75 FU A 2 01/10/2007 30/09/2017 07/5/EC 

Chemical Foramsulfuron HB C 01/07/2003 30/06/2013 03/23/EC 

Chemical Forchlorfenuron PG C 01/04/2006 31/03/2016 06/10/EC 

Chemical Formetanate IN, AC A 2 01/10/2007 30/09/2017 07/5/EC 

Chemical Fosetyl '384 FU A 2 01/05/2007 30/04/2017 06/64/EC 

Chemical Fosthiazate NE C 01/01/2004 31/12/2013 03/84/EC 

Chemical Fuberidazole '525 FU A 3 01/01/2009 31/12/2018 2008/108 

Chemical Glufosinate '437 HB A 2 01/10/2007 30/09/2017 07/25/EC 

Chemical Glyphosate (incl trimesium aka '284 HB A 1 01/07/2002 30/06/2012 01/99/EC 

sulfosate) 

Chemical Imazalil (aka enilconazole) '335 FU A 1 01/01/1999 31/12/2008 97/73/EC 

Chemical Imazamox HB C 01/07/2003 30/06/2013 03/23/EC 

Chemical Imazaquin '699 PG A 3 01/01/2009 31/12/2018 2008/69 

Chemical Imazosulfuron HB C 01/04/2005 31/03/2015 05/3/EC 

Chemical Imidacloprid IN A 3 01/08/2009 31/07/2019 2008/116 

Chemical Indoxacarb IN C 01/04/2006 31/03/2016 06/10/EC 

Chemical Iodosulfuron-methyl-sodium HB C 01/01/2004 31/12/2013 03/84/EC 

Chemical Ioxynil '86 HB A 1 01/03/2005 28/02/2015 04/58/EC 

Chemical Iprodione '278 FU A 1 01/01/2004 31/12/2013 03/31/EC 

Chemical Iprovalicarb FU C 01/07/2002 30/06/2011 02/48/EC 

165


Chemical Iron sulphate HB A 4 01/09/2009 31/08/2019 2008/127 

Chemical Isoproturon '336 HB A 1 01/01/2003 31/12/2012 02/18/EC 

Chemical Isoxaflutole HB C 01/01/2003 31/12/2012 03/68/EC 

Chemical Kresoxim-methyl FU C 01/02/1999 31/01/2009 99/01/EC 

Chemical lambda-Cyhalothrin '463 IN A 1 01/01/2002 31/12/2011 00/80/EC 

Chemical Lenacil '163 HB A 3 01/01/2009 31/12/2018 2008/69 

Chemical Linuron '76 HB A 1 01/01/2004 31/12/2013 03/31/EC 

Chemical Lufenuron IN A 3 01/01/2010 31/12/2019 

Chemical Magnesium phosphide '228 IN, RO A 3 01/09/2009 31/08/2019 2008/125 

Chemical Maleic hydrazide '310 PG A 1 01/01/2004 31/12/2013 03/31/EC 

Chemical Mancozeb '34 FU A 1 01/07/2006 30/06/2016 05/72/EC 

Chemical Maneb '61 FU A 1 01/07/2006 30/06/2016 05/72/EC 

Chemical MCPA '2 HB A 1 01/05/2006 30/04/2016 05/57/EC 

Chemical MCPB '50 HB A 1 01/05/2006 30/04/2016 05/57/EC 

Chemical Mecoprop '51 HB A 1 01/06/2004 31/05/2014 03/70/EC 

Chemical Mecoprop-P '475 HB A 1 01/06/2004 31/05/2014 03/70/EC 

Chemical Mepanipyrim FU C 01/10/2004 30/09/2014 04/62/EC 

Chemical Mepiquat '440 PG A 3 01/01/2009 31/12/2018 2008/108 

Chemical Mesosulfuron HB C 01/04/2004 31/03/2014 03/119/EC 

Chemical Mesotrione HB C 01/10/2003 30/09/2013 03/68/EC 

Chemical Metalaxyl-M FU C 01/10/2002 30/09/2012 02/64/EC 

Chemical Metamitron '381 HB A 3 01/09/2009 31/08/2019 2008/125 

Chemical Metazachlor '411 HB A 3 01/08/2009 31/07/2019 2008/116 

Chemical Metconazole FU A 2 01/06/2007 31/05/2017 06/74/EC 

Chemical Methiocarb (aka 

'165 IN, MO, RE A 2 01/10/2007 30/09/2017 07/5/EC 

mercaptodimethur) 

Chemical Methoxyfenozide IN C 01/04/2005 31/03/2015 05/3/EC 

Chemical Metiram '478 FU A 1 01/07/2006 30/06/2016 05/72/EC 

Chemical Metrafenone FU C 01/02/2007 31/01/2017 07/6/EC 

Chemical Metribuzin '283 HB A 2 01/10/2007 30/09/2017 07/25/EC 

Chemical Metsulfuron '441 HB A 1 01/07/2001 30/06/2011 00/49/EC 

Chemical Molinate '235 HB A 1 01/08/2004 31/07/2014 03/81/EC 

Chemical Nicosulfuron '709 HB A 3 01/01/2009 31/12/2018 2008/40 

Chemical Oxadiargyl HB C 01/07/2003 30/06/2013 03/23/EC 

Chemical Oxadiazon '213 HB A 3 01/01/2009 31/12/2018 2008/69 

Chemical Oxamyl '342 IN, NE A 2 01/08/2006 31/07/2016 06/16/EC 

Chemical Oxasulfuron HB C 01/07/2003 30/06/2013 03/23/EC 

Chemical Penconazole '446 FU A 3 01/01/2010 31/08/2019 

Chemical Pendimethalin '357 HB A 1 01/01/2004 31/12/2013 03/31/EC 

Chemical Pethoxamid HB C 01/08/2006 31/07/2016 06/41/EC 

Chemical Phenmedipham '77 HB A 1 01/03/2005 28/02/2015 04/58/EC 

Chemical Phosmet '318 IN A 2 01/10/2007 30/09/2017 07/25/EC 

Chemical Picloram '174 HB A 3 01/01/2009 31/12/2018 2008/69 

Chemical Picolinafen HB C 01/10/2002 30/09/2012 02/64/EC 

Chemical Picoxystrobin FU C 01/01/2004 31/12/2013 03/84/EC 

Chemical Pirimicarb '231 IN A 2 01/02/2007 31/01/2017 06/39/EC 

Chemical Pirimiphos-methyl '239 IN A 2 01/10/2007 30/09/2017 07/52/EC 

Chemical Prohexadione-calcium PG C 01/10/2000 01/10/2010 00/50/EC 

Chemical Propamocarb '399 FU A 2 01/10/2007 30/09/2017 07/25/EC 

Chemical Propaquizafop HB A 3 01/12/2009 30/11/2019 

Chemical Propiconazole '408 FU A 1 01/06/2004 31/05/2014 03/70/EC 

Chemical Propineb '177 FU A 1 01/04/2004 30/03/2014 03/39/EC 

Chemical Propoxycarbazone HB C 01/04/2004 31/03/2014 03/119/EC 

Chemical Propyzamide '315 HB A 1 01/04/2004 30/03/2014 03/39/EC 

166

Appendix 10 

Chemical Prosulfocarb '539 HB A 3 01/01/2009 31/12/2018 2007/76 

Chemical Prosulfuron HB C 01/07/2002 30/06/2011 02/48/EC 

Chemical Prothioconazole FU C 01/08/2008 31/07/2018 08/44/EC 

Chemical Pymetrozine IN C 01/11/2001 31/10/2011 01/87/EC 

Chemical Pyraclostrobin FU, PG C 01/06/2004 31/05/2014 04/30/EC 

Chemical Pyraflufen-ethyl HB C 01/11/2001 31/10/2011 01/87/EC 

Chemical Pyridate '447 HB A 1 01/01/2002 31/12/2011 01/21/EC 

Chemical Pyrimethanil FU A 2 01/06/2007 31/05/2017 06/74/EC 

Chemical Pyriproxyfen '715 IN A 3 01/01/2009 31/12/2018 2008/69 

Chemical Quinoclamine '648 HB, AL A 3 01/01/2009 31/12/2018 2008/66 

Chemical Quinoxyfen FU C 01/09/2004 31/08/2014 04/60/EC 

Chemical Quizalofop-P '641 HB A 3 01/12/2009 30/11/2019 SCoFCAH 

voted 

01.2009 

Chemical Quizalofop-P-ethyl '641 HB A 3 01/12/2009 30/11/2019 

Chemical Quizalofop-P-tefuryl '641 HB A 3 01/12/2009 30/11/2019 

Chemical Rimsulfuron (aka renriduron) HB A 2 01/02/2007 31/01/2017 06/39/EC 

Chemical Silthiofam FU C 01/01/2004 31/12/2013 03/84/EC 

Chemical S-Metholachlor HB C 01/04/2005 31/03/2015 05/3/EC 

Chemical Sodium 5-nitroguaiacolate PG A 3 01/11/2009 31/10/2019 2009/11 

chemical Sodium hypochlorite BA A 4 01/09/2009 31/08/2019 2008/127 

Chemical Sodium o-nitrophenolate PG A 3 01/11/2009 31/10/2019 2009/11 

Chemical Sodium p-nitrophenolate PG A 3 01/11/2009 31/10/2019 2009/11 

Chemical Spiroxamine FU C 01/09/1999 01/09/2009 99/73/EC 

Chemical Sulcotrione HB A 3 01/09/2009 31/08/2019 2008/125 

Chemical Sulfosulfuron HB C 01/07/2002 30/06/2011 02/48/EC 

Chemical Sulphur '0018 FU, AC, RE A 4 SCoFCAH 

voted 

03.2009 

Chemical Tebuconazole '494 FU A 3 01/09/2009 31/08/2019 2008/125 

Chemical Tebufenpyrad AC A 3 01/11/2009 31/10/2019 2009/11 

Chemical Teflubenzuron '450 IN A 3 01/12/2009 30/11/2019 

Chemical Tepraloxydim HB C 01/06/2005 31/05/2015 05/34/EC 

Chemical Thiabendazole '323 FU A 1 01/01/2002 31/12/2011 01/21/EC 

Chemical Thiacloprid IN C 01/01/2005 31/12/2014 04/99/EC 

Chemical Thiamethoxam IN C 01/02/2007 31/01/2017 07/6/EC 

Chemical Thifensulfuron-methyl '452 HB A 1 01/07/2002 30/06/2012 01/99/EC 

Chemical Thiophanate-methyl '262 FU A 1 01/03/2006 28/02/2016 05/53/EC 

Chemical Thiram '24 FU A 1 01/08/2004 31/07/2014 03/81/EC 

Chemical Tolclofos-methyl '479 FU A 2 01/02/2007 31/01/2017 06/39/EC 

Chemical Tolylfluanid '275 FU, AC A 2 01/10/2006 30/09/2016 06/06/EC 

Chemical Tralkoxydim '544 HB A 3 01/01/2009 31/12/2018 2008/107 

Chemical Triadimenol '398 FU A 3 01/09/2009 31/08/2019 2008/125 

Chemical Tri-allate '97 HB A 3 01/01/2010 31/12/2019 

Chemical Triasulfuron '480 HB A 1 01/08/2001 31/07/2011 00/66/EC 

Chemical Tribasic copper sulfate FU A 3 

Chemical Tribenuron (aka metometuron) '546 HB A 2 01/03/2006 28/02/2016 05/54/EC 

Chemical Triclopyr '376 HB A 2 01/06/2007 31/05/2017 06/74/EC 

Chemical Trifloxystrobin FU C 01/10/2003 30/09/2013 03/68/EC 

Chemical Triflusulfuron HB A 3 01/01/2010 31/12/2019 

Chemical Trinexapac (aka cimetacarb ethyl) PG A 2 01/05/2007 30/04/2017 06/64/EC 

Chemical Triticonazole '652 FU A 2 01/02/2007 31/01/2017 06/39/EC 

Chemical Tritosulfuron HB C 01/12/2008 30/11/2018 08/70/EC 

Chemical Warfarin (aka coumaphene) '70 RO A 1 01/10/2006 30/09/2013 06/05/EC 

167


Chemical zeta-Cypermethrin IN A 3 01/12/2009 30/11/2019 

Chemical Ziram '31 FU, RE A 1 01/08/2004 31/07/2014 03/81/EC 

Chemical Zoxamide FU C 01/04/2004 31/03/2014 03/119/EC 

Chemical 

repellent 

Denathonium benzoate RE A 4 01/09/2009 31/08/2019 2008/127 

Chemical 

repellent 

Chemical 

repellent 

Repellents by smell/ Tall oil crude 

(CAS 8002-26-4) 

Repellents by smell/Tall oil pitch 

(CAS 8016-81-7) 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

Microbial Ampelomyces quisqualis strain 

FU C 01/04/2005 31/03/2015 05/2/EC 

AQ10 

Microbial Bacillus subtilis str. QST 713 BA, FU C 01/02/2007 31/01/2017 07/6/EC 

Microbial 

Microbial 

Microbial 

Microbial 

Bacillus thuringiensis subsp. 

aizawai (ABTS-1857 and GC-91) 


israelensis (AM65-52) 


kurstaki (ABTS 351, PB 54, SA 

11, SA12 and EG 2348) 


tenebrionis (NB 176) 

Microbial Beauveria bassiana (ATCC 74040 

and GHA) 

[IN] A 4 01/01/2009 31/12/2018 2008/113 

[IN] A 4 01/01/2009 31/12/2018 2008/113 

[IN] A 4 01/01/2009 31/12/2018 2008/113 

[IN] A 4 01/01/2009 31/12/2018 2008/113 

IN A 4 01/01/2009 31/12/2018 2008/113 

Microbial Coniothyrium minitans FU C 01/01/2004 31/12/2013 03/79/EC 

Microbial 

Microbial 

Microbial 

Microbial 

Microbial 

Cydia pomonella granulosis virus 

(CpGV) 

Gliocladium catenulatum strain 

J1446 

Lecanicillimum muscarium (Ve6) 

(former Verticillium lecanii) 


(BIPESCO 5F/52) 

Paecilomyces fumosoroseus 

Apopka strain 97 

IN A 4 01/01/2009 31/12/2018 2008/113 

FU C 01/04/2005 31/03/2015 05/2/EC 

IN A 4 01/01/2009 31/12/2018 2008/113 

IN A 4 01/01/2009 31/12/2018 2008/113 

FU C 01/07/2001 30/06/2011 01/47/EC 

Microbial Paecilomyces lilacinus FU C 01/08/2008 31/07/2018 2008/44/EC 

Microbial Phlebiopsis gigantea (several 

FU A 4 01/01/2009 31/12/2018 2008/113 

strains) 

Microbial Pseudomonas chlororaphis 

strain MA342 

FU C 01/10/2004 30/09/2014 04/71/EC 

Microbial Pythium oligandrum (M1) FU A 4 01/01/2009 31/12/2018 2008/113 

Microbial Spodoptera exigua nuclear 

FU C 01/12/2007 30/11/2017 07/50/EC 

polyhedrosis virus 

Microbial 

Streptomyces K61 (K61) (formerly 

Streptomyces griseoviridis) 

Microbial Trichoderma aspellerum (ICC012) 

(T11) (TV1) (formerly T. 

harzianum) 

Microbial Trichoderma atroviride (IMI 

206040) (T 11) (formerly 

Trichoderma harzianum) 

Microbial Trichoderma gamsii (formerly T. 

viride) (ICC080) 

Microbial 

Microbial 

Microbial 

Trichoderma harzianum Rifai (T- 

22) (ITEM 908) 

Trichoderma polysporum (IMI 

206039) 

Verticillium albo-atrum 

(WCS850) (formerly V. dahliae) 

FU A 4 01/01/2009 31/12/2018 2008/113 

FU A 4 01/01/2009 31/12/2018 2008/113 

FU A 4 01/01/2009 31/12/2018 2008/113 

FU A 4 01/01/2009 31/12/2018 2008/113 

FU A 4 01/01/2009 31/12/2018 2008/113 

FU A 4 01/01/2009 31/12/2018 2008/113 

FU A 4 01/01/2009 31/12/2018 2008/113 

168

Appendix 10 

Natural other Abamectin (aka avermectin) '495 AC, IN A 3 01/01/2009 31/12/2018 2008/107 

Natural other Acetic acid HB A 4 01/09/2009 31/08/2018 2008/127 

Natural other Aluminium silicate (aka kaolin) RE A 4 01/09/2009 31/08/2019 2008/127 

Natural other Blood meal RE A 4 01/09/2009 31/08/2019 2008/127 

Natural other Carbon dioxide IN, RO A 4 01/09/2009 31/08/2019 2008/127 

Natural other Fat distilation residues RE A 4 01/09/2009 31/08/2019 2008/127 

Natural other Ferric phosphate MO C 01/11/2001 31/10/2011 01/87/EC 

Natural other Kieselguhr (diatomaceous earth) IN A 4 01/09/2009 31/08/2019 2008/127 

Natural other Milbemectin IN, AC C 01/12/2005 30/11/2015 05/58/EC 

Natural other Quartz sand RE A 4 01/09/2009 31/08/2019 2008/127 

Natural other Spinosad IN C 01/02/2007 31/01/2017 07/6/EC 

Natural other 

by synthesis 

Natural other 

by synthesis 

Natural other 

by synthesis 

Natural other 

fatty acid 

Natural other 

fatty acid 

Natural other 

fatty acid 

Natural other 

fatty acid 

Benzoic acid BA, FU, OT C 01/06/2004 31/05/2014 04/30/EC 

Potassium hydrogen carbonate FU A 4 01/09/2009 31/08/2019 2008/127 

Urea IN A 4 01/09/2009 31/08/2019 2008/127 

Capric acid (CAS 334-48-5) 

Caprylic acid (CAS 124-07-2) 

Fatty acids C7 to C20 

Fatty acids C7-C18 and C18 

unsaturated potassium salts (CAS 

67701-09-1) 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

Natural other 

fatty acid 

Natural other 

fatty acid 

Natural other 

fatty acid 

Natural other 

fatty acid 

Natural other 

fatty acid 

Natural other 

fatty acid 

Natural other 

repellent 

Natural other 

repellent 

Natural other 

Repellent 

Natural other 

repellent 

Natural other 

repellent 

Natural other 

repellent 

Fatty acids C8-C10 methyl esters 

(CAS 85566-26-3) 

Lauric acid (CAS 143-07-7) 

Methyl decanoate (CAS 110-42-9) 

Methyl octaonate (CAS 111-11-5) 

Oleic acid (CAS 112-80-1) 

Pelargonic acid (CAS 112-05-0) 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

IN, AC, HB, 

PG 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

A 4 01/09/2009 31/08/2019 2008/127 

Calcium carbonate RE A 4 01/09/2009 31/08/2019 2008/127 

Limestone RE A 4 01/09/2009 31/08/2019 2008/127 

Methyl nonyl ketone √ RE A 4 01/09/2009 31/08/2019 2008/127 

Sodium aluminium silicate RE A 4 01/09/2009 31/08/2019 2008/127 

Repellents by smell/Fish oil RE A 4 01/09/2009 31/08/2019 2008/127 

Repellents by smell/Sheep fat RE A 4 01/09/2009 31/08/2019 2008/127 

169


Semio (Z)-13-Hexadecen-11yn-1-yl 

2008/127 

acetate √ AT A 4 01/09/2009 31/08/2019 

Semio (Z,Z,Z,Z)-7,13,16,19- 

2008/127 

Docosatetraen-1-yl isobutyrate 

√ AT A 4 01/09/2009 31/08/2019 

Semio Ammonium acetate √ AT A 4 01/01/2009 31/12/2018 2008/127 

Semio Hydrolysed proteins √ IN A 4 01/09/2009 31/08/2019 2008/127 

Semio Putrescine (1,4-Diaminobutane) √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio Trimethylamine hydrochloride √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio Straight Chain Lepidoptera 

Pheromones 

√ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (2E, 13Z)-Octadecadien-1-yl √ AT A 4 01/09/2009 31/08/2019 2008/127 

acetate 

Semio/SCLP (7E, 9E)-Dodecadien 1-yl acetate √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (7E, 9Z)-Dodecadien 1-yl acetate √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (7Z, 11E)-Hexadecadien-1-yl √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

acetate 

Semio/SCLP (7Z, 11Z)-Hexadecdien-1-yl √ AT A 4 01/09/2009 31/08/2019 2008/127 

acetate 

Semio/SCLP (9Z, 12E)-Tetradecadien-1-yl √ AT A 4 01/09/2009 31/08/2019 2008/127 

acetate 

Semio/SCLP (E)-11-Tetradecen-1-yl acetate √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (E)-5-Decen-1-ol √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (E)-5-Decen-1-yl-acetate √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (E)-8-Dodecen-1-yl acetate √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (E,E)-8,10-Dodecadien-1-ol √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (E/Z)-8-Dodecen-1-yl acetate √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-11-Hexadecen-1-ol √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-11-Hexadecen-1-yl acetate √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-11-Hexadecenal √ √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-11-Tetradecen-1-yl acetate √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-13-Octadecenal √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-7-Tetradecenal √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-8-Dodecen-1-ol √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-8-Dodecen-1-yl acetate √ √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-9-Dodecen-1-yl acetate 422 √ AT A 4 01/09/2009 31/08/2019 2008/127 

√ 

Semio/SCLP (Z)-9-Hexadecenal √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP (Z)-9-Tetradecen-1-yl acetate √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP Dodecyl acetate √ √ AT A 4 01/09/2009 31/08/2019 2008/127 

Semio/SCLP Tetradecan-1-ol √ AT A 4 01/09/2009 31/08/2019 2008/127 

Official Total Included: 334 A: Existing active substances divided into 

four lists for phased evaluations 

C: New active substances 

170

Appendix 11. Invertebrate beneficials available as biological control agents against 

invertebrate pests in five European countries. 

11.1. Invertebrate biocontrol agents used in France 

Beneficial Taxonomy Target Crop 

Adalia bipunctata coleoptera aphids on leaves orchards: all 

Adalia bipunctata coleoptera aphids on leaves 

vegetable greenhouse: all 

crops 

Delphastus pusillus coleoptera whiteflies 

vegetables greenhouse 

and covered 

Harmonia axyridis coleoptera aphids on leaves Vegetables , orchards 

Aphidoletes aphidimyza diptera aphids on leaves 

vegetable greenhouse: 

tomato, 

cucumber, egg plant, 

sweet pepper 

Feltiella acarisuga diptera Tetranychus urticae 


crops 

Anthocoris nemoralis heteroptera psylla orchard: pear 

Aleurodina (whiteflies), 

secondarily against 

Macrolophus 


heteroptera Tetranychus & aphids 

caliginosus 

crops 

(Macrosiphum euphorbiae, 

Aphis gossypii) 

Anagrus atomus 

hymenoptera 

Tomato Leaf-hopper 

(Hauptidia maroccana) 

Aphelinus abdominalis hymenoptera aphids: M. euphorbiae 

Aphidius colemani 

hymenoptera 

aphids: 

A. gossypii, Myzus persicae 

(green peach aphid) 

aphids: Aulacorthum solani, M. 

euphorbiae, M. persicae 

171 

vegetables 

vegetable greenhouse: all, 

tomato, 

egg plant, sweet pepper 


crops 

Aphidius ervi 

hymenoptera 


crops 

Diaeretiella rapae hymenoptera aphids : Brevicoryne brassicae Cabbage, oil-seed rape 

Dacnusa sibirica 

Diglyphus isaea 

hymenoptera 

hymenoptera 

Agromyzidae (leaf-miner 

flies) 

Agromyzidae (leaf-miner 

flies) 

Encarsia formosa hymenoptera Aleurodina (whiteflies) 

Eretmocerus eremicus 

(syn. Californicus) 

Eretmocerus mundus 

Orius insidiosus 

hymenoptera 

hymenoptera 

hymenoptera 

Aleurodina (whiteflies): 

Bemisia tabaci, 

Trialeurodes vaporariorum 


B. tabaci, 

T. vaporariorum 

thrips: 

Frankliniella occidentalis, 

Thrips tabaci 

Orius laevigatus hymenoptera thrips, partial: Tetranychus 

Orius majusculus hymenoptera thrips, partial: Tetranychus 


crops 


crops 


crops 


crops 


crops, orchards 


crops 


crops 


crops


Trichogramma brassicae 

Ostrinia nubilalis 

hymenoptera 

Bezdenko 

(European corn borer) 

maize 

Trichogramma 

Noctuidae(Owlet moths), vegetable greenhouse: all 

hymenoptera 

evanescens 

Pyralidae 

crops 

Amblyseius andersoni mite N. rubi, P. ulmi, T.urticae orchards: all 

Amblyseius andersoni mite 

Aculops lycopersici, 

Tetranychus 

Vegetables 

Amblyseius californicus mite Tetranychus, Panonychus vegetables 

Amblyseius cucumeris mite Tetranychus, thrips 

vegetable covered: 

tomato, cucumber, 

sweet pepper, all crops 

(thrips) 

Amblyseius degenerans mite thrips 

vegetable greenhouse: egg 

plant, sweet pepper 

Amblyseius swirskii mite thrips, whiteflies vegetables 

Hypoaspis aculeifer mite 

Sciaridae (fungus gnats), bulb vegetable greenhouse: all 

mite (Rhyzogliphus robini) crops 

Hypoaspis miles mite Sciaridae (fungus gnats), thrips 


crops 

Phytoseiulus persimilis mite Tetranychus urticae vegetables 

Otiorhynchus salicicola, 


nematode Otiorhynchus sulcatus (vine 


weevil), Phyllopertha horticola 

orchards: crops & nursery 

Heterorhabditis megidis nematode 


Otiorhynchus sulcatus (vine Vegetables, flowers 

weevil) 

Phasmarhabditis 

nematode Limacidae (Slugs) vegetable: general 

hermaphrodita 

Steinernema 

carpocapsae 

Steinernema kraussei 

Steinernema 

carpocapsae 

nematode Codling moth pome fruit 

nematode 

nematode 


Otiorhynchus sulcatus (vine 

weevil) 

Noctuids, 

Gryllotalpa gryllotalpa 

(European mole cricket), 

Tipula paludosa (March crane 

fly ) 

vegetable: general 


Steinernema feltiae nematode codling moth, Cydia molesta pome fruit 

Steinernema feltiae nematode Sciaridae (fungus gnats) 

vegetable: general young 

plants 

Chrysoperla carnea nevroptera aphids on leaves 

vegetables and ornements 

covered 

Chrysoperla lucasina 

nevroptera 

aphids, thrips, scales, 

whiteflies, acarids eggs, leak 

moth 

Micromus angulatus nevroptera scales, aphids vegetables 

Franklinothrips 

vespiformis 

thysanoptera thrips 


covered 


crops 

172

Appendix 11 

11.2. Invertebrate biocontrol agents used in Germany 

Beneficial 

Entomopathogenic nematodes 

Heterorhabditis bacteriophora Poinar 

Heterorhabditis megidis Poinar 

Steinernema carpocapsae Weiser 

Steinernema feltiae Filipjev 

Steinernema kraussei Steiner 

Gastropod pathogenic nematodes 

Phasmarhabditis hermaphrodita A. Schneider 

Predatory mites 

Amblyseius andersoni Chant 

Amblyseius barkeri Hughes 

Amblyseius californicus McGregor 

Amblyseius cucumeris Oudemans 

Amblyseius degenerans Berlese 

Amblyseius swirskii Athias-Henriot 

Cheyletus eruditus Schrank 

Hypoaspis aculeifer Canestrini 

Hypoaspis milesBerlese 

Phytoseiulus persimilis Athias-Henriot 

Typhlodromus pyri Scheuten 

Predatory thrips (Thysanoptera) 

Franklinothrips vespiformis Crawford 

Parasitic wasps (Hymenoptera) 

Anagrus atomus Linnaeus 

Anagyrus fusciventris Girault 

Anisopteromalus calandrae Howard 

Aphelinus abdominalis Dalman 

Aphelinus mali Haldeman 

Aphidius colemani Viereck 

Aphidius ervi Haliday 

Aphidius matricariae Haliday 

Aprostocetus hagenowii Ratzeburg 

Cephalonomia tarsalis Ashmead 

Coccidoxenoides perminutus Girault 

Coccophagus licymnia Walker 

Coccophagus rusti Compere 

Pest 

Larvae of vine weevil (Otiorynchus sulcatus), caterpillars 

of ghost moths (genus: Hepialus), larvae of garden 

chaffer (Phyllopertha horticola) and other insect larvae 

feeding on roots 

Larvae of vine weevil (Otiorynchus sulcatus) and other 

insect larvae feeding on roots 

Larvae of vine weevil (Otiorynchus sulcatus) and other 

insect larvae feeding on roots, mole cricket 

Larvae of fungus gnats (Diptera: Sciaridae) and March 

flies (Diptera: Bibionidae) 

Insect larvae feeding on roots, e.g. vine weevil 

(Otiorynchus sulcatus) 

Slugs (Deroceras spp, Agriolimax spp and others) 

Spider mites (Tetranychus spp, Panonychus spp), gall 

mites (Eriophyidae) u.a. 

Thrips (Frankliniella occidentalis and others) 

Spider mites 

Thrips (Frankliniella occidentalis and others) 

Thrips 

White flies (e.g. Bemisia tabaci), 

spider mites (Tetranychus spp.) and thrips 

Stored product mites, booklice (Psocoptera) 

Thrips 

Thrips 

Spider mites (Tetranychus spp) 

Spider mites 

Thrips (in particular Echinothrips americanus, 

Parthenothrips dracaenae, Frankliniella occidentalis) 

Cicadidae eggs 

Wooly aphids (Eriosomatidae) and mealy bugs 

(Pseudococcididae) 

Drugstore (Stegobium paniceum), Tobacco (Lasioderma 

serricorne) 

Aphids (Macrosiphum euphorbiae, Aulacorthum solani) 

Wooly aphid (Eriosoma lanigerum) 

Aphids (Aphis gossypii, Myzus persicae, M. nicotianae) 

Aphids (Macrosiphum euphorbiae) 

Aphids (Myzus persicae) 

Cockroaches (Blatta orientalis, Periplaneta spp) 

Saw-toothed and marchand grain beetles (Oryzaephilus 

surinamensis und O. mercator) 

Different wooly aphids and mealy bugs 


Scale insects (Coccidae) 


173


Coccophagus scutellaris Dalman 

Dacnusa sibirica Telenga 

Diglyphus isaea Walker 

Diaeretiella rapae M'Intosh 

Encarsia citrina Craw 

Encarsia formosa Gahan 

Encyrtus lecaniorum Mayr 

Eretmocerus californicus Howard (= eremicus 

Rose & Zolnerowich) 

Eretmocerus mundus Mercet 

Gyranusoidea litura Prinsloo 

Habrobracon hebetor Say 

Lariophagus distinguendus Förster 

Leptomastidea abnormis Girault 

Leptomastix dactylopii Howard 

Leptomastix epona 

Walker 

Lysiphlebus testaceipes Cresson 

Metaphycus flavus Howard 

Metaphycus helvolus Compere 

Metaphycus lounsburyi Howard 

Metaphycus stanleyi Compere 

Microterys flavus Howard 

Pseudaphycus maculipennis Mercet 

Theocolax elegans Westwood 

Thripobius semiluteus Boucek 


Bezdenko 

Trichogramma cacoeciae Marchal 

Trichogramma dendrolimi Matsumura 

Trichogramma evanescens Westwood 

Trichogramma evanescens Westwood (Stamm 

„Lager“) 

Venturia canescens Gravenhorst 

Predatory midges and syrphids (Diptera) 

Aphidoletes aphidimyza Rondani 

Diaeretiella rapae DeGeer 

Feltiella acarisuga Vallot 

Predatory beetles (Coleoptera) 

Adalia bipunctata Linnaeus 

Atheta coriaria Kraatz 

Chilocorus nigritus Fabricius 


Leaf-miner flies (Agromyzidae: Liriomyza and others 

Leaf-miner flies (Agromyzidae: Liriomyza and others 

Cabbage aphid (Brevicoryne brassicae) 

Diaspididae 

White fly (Trialeurodes vaporarium) 

Scale insect (Saissetia hemisphaerica) 

White flies (Bemisia spp and others) 

White flies (Aleyrodidae) 

Long-tailed mealy bug (Pseudococcus longispinus) 

Stored product moths (Indian Meal moth, Plodia 

interpuntella) and (Ephestia spp) 

Grain weevils (Sitophilus spp), drugstore beetle 

(Stegobium paniceum), tobacco beetle (Lasioderma 

serricorne), shiny spider beetle (Gibbium psylloides), 

golden spider beetle (Niptus hololeucus) 

Wooly aphids and mealy bugs (Pseudococcididae) 



Apids (Aphis gossypii) 

Scale insects (Coccidae: Saissetia oleae, Coccus 

hesperidum) 

Scale insects (Coccidae: Saissetia oleae, 

Coccus hesperidum) 

Scale insects (Coccidae: Saissetia oleae) 


Scale insects (Coccidae: Saissetia oleae) 


Lesser grain borer (Rhyzopertha dominica) 

Thrips (Hercinothrips femoralis, Heliothrips 

haemorrhoidalis, Echinothrips americanus) 

Eggs of corn borer (Ostrinia nubilalis) and other moths 

Eggs of plum maggot moth (Cydia funebrana) and 

codling moth (Cydia pomonella) 

Eggs of plum maggot moth (Cydia funebrana) and 

codling moth (Cydia pomonella) 

Eggs of pest lepidoptera and stored product moths 

Eggs of stored product moths 

Eggs of stored product mothes (Indian meal moth, Plodia 

interpuntella) and (Ephestia spp) 

Aphids 

Aphids 

Spider mites (Tetranychus urticae, T. cinnabarinus, 

Panonychus ulmi) 

Aphids 

Parasites of fly pupa 

Scale insects 

174

Appendix 11 

Coccinella septempunctata Linnaeus 

Cryptolaemus montrouzieri Mulsant 

Exochomus quadripustulatus Linnaeus 

Rhyzobius forestieri Mulsant 

Rhyzobius lophantae Blaisdell 

Rodolia cardinalis Mulsant 

Stethorus punctillum Weise 

Predatory true bugs (Heteroptera) 

Anthocoris nemoralis Fabricius 

Dicyphus hesperus Knight 

Macrolophus melanotoma Costa(= caliginosus 

E. Wagner) 

Macrolophus pygmaeus Rambur 

Orius insidiosus Say 

Orius laevigatus Fieber 

Orius majusculus Reuter 

Lacewings 

Chrysoperla carnea Stephens 

Parasites and predators of stable flies 

Diaeretiella rapae Girault & Sanders 

Muscidifurax zaraptor Kogan & Legner 

Nasonia vitripennis Walker 

Spalangia cameroni Perkins 

Spalangia endius Walker 

Spalangia nigroaeneus Curtis 

Hydrothaea aenescens Wiedemann 

Aphids 



Scale insects 

Scale insects (Saissetia oleae) 

Scale insects (Coccidae), Wooly aphids (Eriosomatidae) 

and mealy bugs (Pseudococcididae) 



Spider mites 

Suckers (Psyllids, Psyllidae) 

White fly (Trialeurodes vaporariorum) 



Thrips (Thysanoptera) 



Aphids 

Housefly-related flies 







Source: http://www.jki.bund.de/ 

175


11.3. Invertebrate biocontrol agents used in Spain 


Adalia bipunctata coleoptera Aphids on leaves orchards: all 

Adalia bipunctata coleoptera Aphids on leaves 


crops 

Delphastus pusillus coleoptera Whiteflies 




Aphidoletes aphidimyza diptera Aphids on leaves 


tomato, 


sweet pepper 



crops 

Anthocoris nemoralis heteroptera Psylla orchard: pear 


secondary vs 

Macrolophus 


heteroptera Tetranychus & 

caliginosus 

crops 

Aphids: Macrosiphum 

euphorbiae, Aphis gossypii 

Anagrus atomus hymenoptera 


vegetables 

Aphelinus abdominalis 

hymenoptera 


Aphids: 

Macrosiphum 

euphorbiae 

Aphids: 

Aphis gossypii, 

176 


tomato, 


Aphidius colemani hymenoptera 


crops 

Myzus persicae (green peach 

aphid) 

Aphidius ervi 

hymenoptera 

Aphids: Aulacorthum solani 


Macrosiphum euphorbiae, 

crops 

myzus persicae 

Diaeretiella rapae hymenoptera Aphids : Brevicoryne brassicae Cabbage, oil-seed rape 

Dacnusa sibirica hymenoptera 

Agromyzidae 


(leaf-miner flies) 

crops 

Diglyphus isaea hymenoptera 

Agromyzidae 



crops 

Encarsia formosa hymenoptera Aleurodina (whiteflies) 



Eretmocerus mundus 

Orius insidiosus 

Orius laevigatus 

Orius majusculus 

hymenoptera 

hymenoptera 

hymenoptera 

hymenoptera 

hymenoptera 







Thrips: 


Thrips tabaci 

Thrips, 

partial: Tetranychus 

Thrips, 



crops 


crops 


crops, orchards 


crops 


crops 


crops

Appendix 11 


Ostrinia nubilalis 

hymenoptera 

Bezdenko 


maize 



hymenoptera 

Bezdenko 

Pyralidae 

crops 

Trichogramma 


hymenoptera 

evanescens 

Pyralidae 

crops 

Amblyseius andersoni mite N. rubi, P. ulmi, T.urticae orchards: all 

Amblyseius andersoni mite 

Aculops lycopersici, 

Tetranychus 

Vegetables 

Amblyseius californicus mite Tetranychus, Panonychus vegetables 

Amblyseius cucumeris mite Tetranychus, thrips 

vegetable covered: 



(thrips) 

Amblyseius degenerans mite Thrips 

vegetable greenhouse: egg 


Amblyseius barkeri 

(mackenziei) 

mite Thrips vegetables 

Amblyseius swirskii mite Thrips, whiteflies vegetables 

Hypoaspis aculeifer mite 

Sciaridae (fungus gnats), bulb vegetable greenhouse: all 

mite (Rhyzogliphus robini) crops 

Hypoaspis miles mite Sciaridae (fungus gnats), thrips 


crops 

Phytoseiulus persimilis mite Tetranychus urticae vegetables 



nematode Otiorhynchus sulcatus (vine 


weevil),Phyllopertha horticola 

orchards: crops & nursery 

Heterorhabditis megidis nematode 


Otiorhynchus sulcatus (vine Vegetables, flowers 

weevil) 



hermaphrodita 

Steinernema 

carpocapsae 

Steinernema kraussei 

Steinernema 

carpocapsae 

nematode Codling moth Apple, pear 

nematode 

nematode 



weevil) 

Noctuids, 


(European mole cricket), 

Tipula paludosa (March crane 

fly ) 

177 



Steinernema feltiae nematode Codling moth, cydia molesta Apple, pear 

Steinernema feltiae nematode Sciaridae (fungus gnats) 

vegetable: general young 

plants 

Chrysoperla carnea nevroptera aphids on leaves 


covered 

Chrysoperla lucasina 

nevroptera 

Aphids, thrips, scales, 

whiteflies, acarids eggs, leak 

moth 


covered 

Micromus angulatus nevroptera Scales, aphids vegetables 

Franklinothrips 


Thrips 

Thrips 

vespiformis 

crops 


Adalia bipunctata coleoptera Aphids on leaves vegetable greenhouse: all


crops 

Delphastus pusillus coleoptera Whiteflies 




Aphidoletes aphidimyza diptera Aphids on leaves 


tomato, cucumber, egg 




crops 



secondary vs 

Macrolophus 


heteroptera Tetranychus & 

caliginosus 

crops 



Anagrus atomus hymenoptera 


vegetables 

Aphelinus abdominalis 

hymenoptera 


Aphids: 

Macrosiphum 

euphorbiae 


tomato, egg plant, sweet 

pepper 

178

Appendix 11 

11.4. Invertebrate biocontrol agents used in Switzerland 



Adalia bipunctata coleoptera Aphids on leaves vegetable greenhouse: egg 

plant, cucumber, sweet 

pepper 

Aphidoletes aphidimyza diptera Aphids on leaves vegetable greenhouse: 

tomato, 


sweet pepper 

Aphidoletes aphidimyza diptera Aphids on leaves vegetable covered: all 

Feltiella acarisuga diptera Tetranychus urticae vegetable greenhouse: 


sweet pepper 


Macrolophus 

caliginosus 

heteroptera 


secondary vs 

Tetranychus & 



Aphelinus abdominalis hymenoptera Aphids: 

Macrosiphum 

euphorbiae, 

Aulacorthum solani 


aphid) 

Aphidius colemani hymenoptera Aphids: 

Aphis gossypii, 

Aphis fabae, 


aphid) 

hymenoptera 

Aphids: 

Aulacorthum solani 

Macrosiphum euphorbiae 

179 


tomato, 



tomato, 



crops 


crops 

Aphidius ervi 

hymenoptera Agromyzidae 


Dacnusa sibirica 


crops 

hymenoptera Agromyzidae 




crops 

Encarsia formosa hymenoptera Aleurodina (whiteflies) vegetable greenhouse: all 

crops 

hymenoptera Aleurodina (whiteflies): vegetable greenhouse: 


tomato, 

Trialeurodes vaporariorum cucumber, egg plant, 



Orius insidiosus hymenoptera Thrips: 


Thrips tabaci 

sweet pepper 


sweet pepper 

hymenoptera Thrips, 


Orius laevigatus 


crops 

hymenoptera Thrips, 


Orius majusculus 


sweet pepper 

Trichogramma brassicae hymenoptera Ostrinia nubilalis 

maize 

Bezdenko 


Trichogramma brassicae hymenoptera Noctuidae(Owlet moths), vegetable greenhouse: all


Bezdenko Pyralidae crops 

Amblyseius barkeri 

(mackenziei) 

mite Thrips vegetable greenhouse: all 

crops, tomato, cucumber, 


Amblyseius californicus mite Tetranychus vegetable greenhouse: 

sweet pepper 

Amblyseius cucumeris mite Tetranychus, thrips vegetable covered: 



(thrips) 

Amblyseius degenerans mite Tetranychus, thrips vegetable greenhouse: egg 


mite Sciaridae (fungus gnats) vegetable greenhouse: all 

Hypoaspis aculeifer 

crops 

Hypoaspis miles mite Sciaridae (fungus gnats) vegetable greenhouse: all 

crops 

mite 

Phytoseiulus persimilis 

Tetranychus urticae 

Heterorhabditis nematode Otiorhynchus salicicola, 



weevil) 

Heterorhabditis megidis nematode Otiorhynchus salicicola, 


weevil) 

Heterorhabditis megidis nematode Otiorhynchus salicicola, 


weevil) 


hermaphrodita 

Photorhabdus 

luminescens 

Photorhabdus 

luminescens 

Steinernema 

carpocapsae 

Steinernema 

carpocapsae 

Steinernema 

carpocapsae 


crops, tomato, cucumber, 


orchards: nursery 


vine: young plants 


nematode 

nematode 

nematode 

nematode 

nematode 



weevil) 



weevil) 



weevil) 



weevil) 

Noctuids, 


(European mole cricket) 



orchards: all 



Steinernema feltidae nematode Sciaridae (fungus gnats) vegetable: general young 

plants 

Xenorhabdus bovienii nematode Sciaridae (fungus gnats) vegetable: general young 

plants 

180

Appendix 11 

11.5. Invertebrate biocontrol agents used in the United Kingdom 

Active Substance Product Name Type of product Target(s) 

Steinernema feltiae Nemasys 

Entompathogenic Sciarids, leafminer, 

nematode 

WFT 

Steinernema kraussei Nemasys L 

Entompathogenic 

nematode 

vine weevil 

Heterorhabditis megidis Nemasys H 


nematode 

vine weevil, 



nematode 

Grubs 

Steinernema carpocasae Nemasys C 

Entompathogenic codling moth (occasional 

nematode 

cutworms) 

Steinernema carpocasae Nemasys C 


nematode 

Hylobius 


hermaphrodita 

Nemaslug slug parasitic nematode Slugs 

Adalia bipunctata Adalsure Natural enemy Aphids 

Amblyseius californicus Ambsure Natural enemy Thrips, rsm 

Trichogramma evanescans Trichogramma Natural enemy Caterpillars 

Anagrus atomus Anagsure Natural enemy Leaf hopper 

Amblyseius cucumeris Ambsure Natural enemy Thrips 

Hypoaspis miles Hyposure Natural enemy 

181 

Thrips, bulb mite, 

sciarids 

Orius laevigatus Orisure Natural enemy Thrips 

Aphelinus abdominalis Aphelsure Natural enemy Aphids 

Aphidius ervi Aphissure (e) Natural enemy Thrips 

Aphidius colemani Aphisure (c) Natural enemy Thrips 

Aphidoletes aphidimyza Aphidosure Natural enemy Aphids 

Chilocorus nigritus Chilosure(n) Natural enemy Scale insect 

Chrysoperla carnea Chrysosure (c ) Natural enemy Aphids 

Cryptolaemus montrouzieiri Cryptosure (m) Natural enemy Mealy bug 

Dacnusa sibirica Dacsure (si) Natural enemy Leaf miner 

Diglyphus isaea Digsure (i) Natural enemy Leaf miner 

Encarsia formosa Encsure Natural enemy Whitefly 

Encarsia formosa and 

Enersure Natural enemy Whitefly 


Eretmocerus eremicus Eretsure (f) Natural enemy Whitefly 

Feltiella acarisuga Felsure (a) Natural enemy rsm 

Macrolophus caliginosus Macsure (c ) Natural enemy Whitefly 

Phytoseiulus persimilis Phytosure (p) Natural enemy rsm 

Bombus terrestris Beesure Pollinator Pollination 

Metaphycus helvolus, 

Encarsia citrina, 

Coccophagus lycimnia and 

Encyrtus infelix 

Scalesure Natural enemy Scale insect 

Leptomastix dactilopii Leptosure (d) Natural enemy Mealy bug 

Leptomastix dactylopii, 

Anagyrus pseudococci and 

Leptomastidea abnormis 

Mealysure Natural enemy Mealy bug 

Metaphycus helviolus Metasure (h) Natural enemy Scale insect 

Encarsia formosa EN-STRIP parasitic wasp Whitefly 

Encarsia formosa + 

Eretmocerus eremicus pupae 

ENERMIX parasitic wasp Whitefly


Eretmocerus eremicus ERCAL parasitic wasp Whitefly 

Macrolophus caliginosus MIRICAL predatory bug Whitefly/spidermite 

Macrolophus caliginosus MIRICAL NYMPH predatory bug Whitefly/spidermite 

Feltiella acarisuga SPIDEND predatory bug Spidermite 

Phytoseiulus persimilis SPIDEX predatory mite Spidermite 

Amblyseius californicus SPICAL predatory mite Spidermite 

Aphidoletes aphidimyza APHIDEND predatory bug Aphids 

Aphelinus abdominalis APHILIN parasitic wasp Aphids 

Aphidius colemani APHIPAR parasitic wasp Aphids 

Chrysoperla carnea CHRYSOPA predatory bug Aphids 

Aphidius ervi ERVIPAR parasitic wasp Aphids 

Episyrphus balteatus SYRPHIDEND predatory bug Aphids 

Adalia bipunctata ADALIA larvae predatory beetle Aphids 

Amblyseius cucumeris THRIPEX predatory mite Thrips + some mites 

Orius laevigatus THRIPOR predatory bug Thrips 

Amblyseius swirski SWIRSKI MITE predatory mite Thrips and Whiteflies 

Dacnusa sibirica + 


DIMINEX parasitic wasp Leafminers 

Diglyphus isaea MIGLYPHUS parasitic wasp Leafminers 

Dacnusa sibirica MINUSA parasitic wasp Leafminers 

Hypoaspis aculeifer 

ENTOMITE 

aculeifer 

predatory mite 

Sciarids 

Steinernema feltiae ENTONEM parasitic nematode Sciarids 

Steinernema feltiae SCIA-RID parasitic nematode Mushroom flies 


CAPSANEM 50 

million 

parasitic nematode Cranefly, Caterpillar 

Trichogramma sp. TRICHO-STRIP parasitic wasp Caterpillar 

Heterorhabditis megidis LARVANEM parasitic nematode Vine Weevil, Chafer 

Cryptolaemus montrouzieri CRYPTOBUG predatory beetle Mealybug 

Adalia bipunctata Adaline b Predator Aphids 

Amblyseius (Euseius) ovalis Ovaline Predator Whitefly and thrips 

Amblyseius (Iphiseius) 

degenerans 

Amblyline d Predator Thrips 

Amblyseius (Neoseiulus ) 

californicus 

Amblyline cal Predator Spider mites 

Amblyseius (Neoseiulus) 

cucumeris 

Amblyline cu Predator Thrips 

Amblyseius (Typhlodromips) 

montdorensis 

Amblyline m Predator Thrips 

Amblyseius (Typhlodromips) 

swirskii 

Swirskiline Predator Whitefly and thrips 

Amblyseius andersoni Anderline aa Predator Spider mites 

Anagrus atomus Anagline a Parasitoid Leaf Hoppers 

Anthocoris nemoralis Antholine n Predator Pear Psylla 

Aphelinus abdominalis Apheline a Parasitoid Aphids 

Aphidius colemani Aphiline c Parasitoid Small aphids 

Aphidius ervi Aphiline e Parasitoid Large aphids 

Aphidoletes aphidimyza Aphidoline a Predator Aphids 

Atheta coriaria Staphyline c Predator Sciarid and Shore Flies 

Bombus terrestris 

Beeline Total 

System 

Pollinator - 

Chrysoperla carnea Chrysoline c Predator Aphids 

Cryptolaemus montrouzieri Cryptoline m Predator Mealybugs 

Dacnusa sibirica Dacline s Parasitoid Leafminers 

182

Appendix 11 

Diglyphus isaea Digline i Parasitoid Leafminers 

Encarsia formosa Encarline f Parasitoid Trialeurodes 

Eretmocerus eremicus Eretline e Parasitoid 

Trialeurodes and 

Bemisia 

Feltiella acarisuga Feltiline a Predator Spider mites 


Entomopathogenic 

nematode 

Vine Weevils 

Hypoaspis miles Hypoline m Predator Sciarid Flies 

Macrolophus caliginosus 

(also known as M. 

Macroline c Predator Whiteflies 

pygmaeus) 

Orius laevigatus Oriline l Predator Thrips 

Orius majusculus Oriline m Predator Thrips 


Entomopathogenic 

Nemaslug 

hermaphrodita 

nematode 

Slugs 

Phytoseiulus persimilis Phytoline p Predator Spider mites 

183

Nicot, P. C. (Ed) 

Classical and augmentative biological control against diseases and pests: critical status analysis and 

review of factors influencing their success 

1 st Edition August 2011 

Copyright: IOBC/WPRS 20011 

http://www.iobc-wprs.org 

ISBN 978-92-9067-243-2

Classical and augmentative biological control against ... - IOBC-WPRS

You also want an ePaper? Increase the reach of your titles

Delete template?

Save as template?