2 Diseases of Atemoya, Cherimoya, Soursop,

Sugar Apple and Related Fruit Crops

Randy C. Ploetz
University of Florida, Tropical Research and Education Center, Homestead, Florida, USA

Introduction Paull, 1998). It requires hot, humid condi-

tions and is quite sensitive to frost. It is often
The Annonaceae is a large neotropical family a poor producer of fruit and, since it is not
of trees and small shrubs that contains ~75 widely adapted, it is not widely grown. Its
genera (Nakasone and Paull, 1998). Of fruit are comparable with those of cherimoya
these, Annona is the most important. It con- and weigh between 455 and 650 g.
tains ~100 species and the most significant Soursop, A. muricata, originated in the
fruit crops. Martin et al. (1987) listed ten Caribbean and now has a pantropical distri-
species or hybrids of major importance in bution (Nakasone and Paull, 1998). It is the
the family, but only seven of these are most tropical of these crops and demands
grown commercially. hot, high rainfall conditions. It is very sensi-
tive to temperatures below ~5°C, and freez-
ing temperatures usually kill plants. Fruit
The Significant Species set, which can be poor, presumably is related
to frequency of pollination. Fruit weigh from
Cherimoya, A. cherimola, originated in the 1 to 4 kg, are sweet to subacid in taste, and
highlands of Ecuador and Peru, but is now are eaten fresh and used in drinks and
widely grown in the tropics and subtropics desserts. Propagation is primarily by seed,
(Nakasone and Paull, 1998). Since the species but superior genotypes have been selected
requires cool night temperatures for appre- from seedling populations for vegetative
ciable fruit set, it is restricted to tropical propagation in Malaysia and Mexico.
highland and cool subtropical environments. Custard apple or Bullock’s heart, A. retic-
Like many species in the family, it requires ulata, originated in tropical America, but is
hand pollination for good production. The now found throughout the tropics (Martin et
fruit weighs from 200 to 2000 g, is sweet and al., 1987). In some locations, such as
is eaten out of the hand or used in ice creams Australia, the annonaceous fruits are
and sherbets. Propagation is by either seed referred to generically as custard apples. To
or grafting, and superior clones have been avoid confusion in this chapter, custard
selected in Australia, Chile, Ecuador, New apple will refer specifically to A. reticulata.
Zealand, Spain and the USA (California) Custard apple grows under the same types
(Nakasone and Paull, 1998). of conditions that are favoured by soursop,
Ilama, A. diversifolia, originated in western but it tolerates light frost. Its fruit weigh
Mexico and Central America (Nakasone and between 400 and 1000 g, and are used in the

© CAB International 2003. Diseases of Tropical Fruit Crops (ed. R.C. Ploetz) 21
22 R.C. Ploetz

same ways as cherimoya, although their production. Since pond apple grows natu-
flavour is not as good. Cracking of the fruit rally in swampy areas, its use as a rootstock
surface at maturity, a common problem with in poorly drained areas has been suggested.
annonaceous fruit, is particularly severe in Núñez-Elisea et al. (1999) reported that
this species and further limits the mar- scions of the normally flood-sensitive cus-
ketability of these fruit (Paull, 1996). Custard tard apple, ‘Gefner’ atemoya and ‘49–11’
apple is propagated by seed. (‘Gefner’ atemoya ⫻ custard apple) toler-
Sugar apple or sweetsop, A. squamosa, is ated flooding (survived and grew) when
from tropical America and widely distrib- grafted on rootstocks of pond apple, but that
uted in the eastern and western hemi- plants grafted on to rootstocks of sugar
spheres. Its environmental requirements apple and custard apple often died.
mirror those of the custard apple. It pro- Seedlings of pond apple and soursop were
duces a sweet, widely appreciated fruit that also flood tolerant, but seedlings of sugar
is used in a variety of drinks and desserts. apple were not. Based on these results, the
Propagation is by seed or grafting, and authors suggested that the use of pond
selected cultivars are produced in Cuba, apple and soursop rootstocks might enable
India and Taiwan. production in marginal, flood-prone sites.
Atemoya, A. cherimola ⫻ A. squamosa, is However, this recommendation should be
the only important interspecific hybrid in made with caution since pond apple and
this family, and may be the most widely soursop are both susceptible to Phytophthora
adapted of the annonaceous fruit crops palmivora, a pathogen that is most damaging
(Martin et al., 1987). The common name is in poorly drained soils (see below).
derived from the Brazilian names for the
parents, ate for A. squamosa and moya for A.
cherimola. The first hybrids were made in Fruit Attributes
Florida in 1908, and subsequent selections
were made in Australia, India, Israel and The annonaceous fruits are composites of
South Africa (Nakasone and Paull, 1998). many fused, single-seeded fruitlets. They
Several named cultivars are now propagated are climacteric and must be picked when
by grafting in the tropics and subtropics. mature in order to ripen properly
Like sugar apple, but unlike cherimoya, it (Snowdon, 1990). Their storage life is very
bears fruit in warm tropical and subtropical limited and, once fruit begin to soften, it is
situations. It tolerates a wide range of soils usually a matter of days before they must be
and climatic conditions, and survives light consumed. They are sensitive to chilling
frosts. Some clones require hand pollination injury, and are stored optimally at tempera-
for adequate fruit set. Its fruit weigh between tures as high as 20°C. Atemoyas can be
300 and 900 g, have an exceptionally good, stored for up to 2 weeks at 12–15°C.
sweet taste, and are eaten fresh or used in a Ethylene is used to facilitate uniform ripen-
variety of desserts. ing in some commercial situations.
Biriba, Rollinia deliciosa, originated in In general, these fruit tend to split
Brazil and is grown primarily there where it between fruitlets once ripening has
is also known as fruta de condessa (Martin et advanced, and this promotes the develop-
al., 1987). It has the same environmental ment of postharvest diseases (Paull, 1996).
requirements and sensitivities as soursop. Wound sites that are associated with annona
Pond apple, A. glabra, is native to south- seed borers, Brephratelloides spp., are addi-
ern Florida, the Caribbean and the lowlands tional points of entry for these pathogens.
of tropical America. It is not an important
fruit crop, but is mentioned here due to its
potential as a rootstock (Nakasone and Paull, Major and Minor Diseases
1998). Most commercial annonas are sensi-
tive to waterlogged soils and must be A dozen diseases of these crops are dis-
planted in well-drained sites for optimum cussed below. Some, such as anthracnose
 Diseases of Annonaceae 23

and bacterial wilt, can have major impacts mature fruit. Alternatively, maturing or har-
on production and require adequate man- vested fruit can be severely affected by a
agement to ensure commercially viable black, dry rot.
yields. Others, such as black canker, Infections on leaves are first visible as
Diplodia fruit rot and purple blotch, are light green dots that coalesce and darken to a
important problems only under certain con- chestnut or black colour, become circular or
ditions, and specific measures to control elongated, and eventually impart a scorched
them usually are not indicated. The geo- appearance to the canopy (Cook, 1975). In
graphic distributions of these diseases are severe cases, trees defoliate prematurely.
also quite variable, and range from global Lesions on seedlings can girdle the stem and
(anthracnose) to a single state or country cause damping off. Those on shoots in estab-
(bacterial wilt and yellow blotch). lished trees cause desiccation above the
Minor diseases of these crops are listed at lesion and the initiation of adventitious
the end of the chapter (Table 2.1). Diseases shoots below, which, themselves, may then
on this list rarely, if ever, cause important be affected. This recurring damage can lead
problems, and scant descriptive information to a witches’-broom appearance in the
on them exists. The causal agents, affected canopy. Cankers that do not exude gum form
taxa and associated literature references for in chronically damaged areas.
these diseases are listed in Table 2.1.
Causal agents
Anthracnose Glomerella cingulata (anamorph: Colletotrichum
gloeosporioides) is the primary or perhaps only
Anthracnose is among the most common causal agent. C. anonicola (Ciferri and
and damaging diseases of annonaceous González-Fragoso, 1927; Deighton, 1939) and
fruit crops. It can severely limit fruit pro- Gloeosporium anonae (Batista, 1953) are also
duction, and has been reported from reported causes, but were not compared with
Australia, the Azores, Bangladesh, Brazil, C. gloeosporioides to determine whether they
China, Dominican Republic, Egypt, were synonymous. G. cingulata and C.
Mozambique, the Philippines, Puerto Rico, gloeosporioides are described in Chapter 1.
Sierra Leone, Uganda and the USA (Florida
and Hawaii) (Snowden, 1921; Li, 1936;
Epidemiology
Deighton, 1939; Aruda, 1940; DeCarvalho,
1948; Alvarez-García, 1949; Batista, 1953; Although little has been reported on this
Abo-El-Dahab and El-Goorani, 1971; Cook, disease in the above species, it can be
1975; Raabe et al., 1981; Brown et al., 1988; assumed that pathogen behaviour resembles
Snowdon, 1990; Alfieri et al., 1994). In all that on other crops. Conidia are dissemi-
likelihood, anthracnose occurs wherever nated in rainsplash and wind-driven rain,
these crops are grown in warm, humid and germinate and infect under warm,
environments. Atemoya, biriba, cherimoya, moist conditions. Infections are usually
custard apple, ilama, soursop, sugar apple latent on fruit, and do not develop until
and A. marcgravii are affected. ripening begins. Wet conditions promote
disease development and the eventual pro-
duction of conidia on all host tissues.
Symptoms
Although the teleomorph has been found in
Affected flower petals exhibit dark-brown badly rotted fruit, it is not known whether
lesions that enlarge, become black and or to what extent ascospores play a role in
cause flowers to shed, thereby reducing the disease cycle.
fruit set (Cook, 1975). Infections on young The pathogen survives rather well in
fruit cause either rotting and mummifica- dead host debris. Thus, leaves, fruit and old
tion, or the formation of a hardened plug flowers are probably important sources of
and no external symptoms of rotting on inoculum.
24 R.C. Ploetz

Management the bark and along the roots of affected trees,

as do basidiomes (mushrooms or basidio-
Frequent applications of fungicides are
carps) on the soil surface or trunk of affected
needed to control the disease, especially dur-
trees. Basidiome morphology is distinct for
ing wet weather. Applications may be needed
each of the described species (Shaw and Kile,
from flower initiation until harvest, depend-
1991). This and interfertility studies are used
ing on prevailing weather conditions.
to delineate most of the Armillaria species.
Unfortunately, rhizomorphs and basidiomes
may not be produced in tropical and warm
Armillaria (mushroom) root rot
subtropical environments. Identification is
complicated further in homothallic species in
This is a widespread disease that is caused
which individuals produce basidiomes.
by at least three different species of
Armillaria root rot is difficult to control,
Armillaria. In the USA, A. mellea affects cher-
especially now that soil fumigants are
imoya in California and A. socialis affects becoming increasingly scarce. The pathogens
cherimoya and soursop in Florida (Rhoads, can survive long periods as saprophytes and,
1942; Farr et al., 1989). Both species are thus, contaminate soil long after a host has
described in Chapter 1. Although A. mellea died. In addition, they can move consider-
was also reported on soursop in Uganda able distances in soil via their rhizomorphs.
(Small, 1926), recent studies have shown Although removal of all host materials from
that A. mellea senso stricto (heterothallic) is fields prior to planting is a common recom-
not present in Africa, but a species that cul- mendation, in practice it is often not possible
turally resembles A. mellea is (Shaw and to do this effectively (Shaw and Kile, 1991).
Kile, 1991). It is homothallic and partially
sexually compatible with isolates of A. mel-
lea senso stricto but, based on isozyme analy- Bacterial wilt
ses, is distinct enough to be considered a
different species (Mwenje and Ride, 1997). Bacterial wilt causes widespread damage
Although Kile et al. (1994) suggested the epi- and tree mortality in Queensland, Australia
thet A. mellea ssp. africana should be used to (Mayers and Hutton, 1987). Seedlings in
identify this taxon, Mwenje and Ride (1997) nurseries and grafted trees in the field are
felt that it should be referred to as the affected. The disease had been recognized as
African A. mellea group until more definitive basal and root rot since 1918, but its cause
studies were conducted. In Australia, A. remained elusive until the early 1980s. The
luteobubalina is the causal agent (Vock, 1978). above authors speculated that this disease
Based on the disease’s presence on three dif- might be found in other annona-producing
ferent continents and the diversity of causal areas since the causal agent is widely spread.
agents, it is probable that this disease occurs
in other areas.
Symptoms
Shaw and Kile (1991) listed the following
chronological order in which symptoms of Two disease syndromes are recognized
Armillaria root rot develop: reduced canopy (Persley, 1993). Young plants or seedlings
growth; chlorosis, stunting of foliage and wilt rapidly and die during the summer and
defoliation; canopy dieback; stress-induced autumn. This occurs mainly on plants within
increase in fruit production; appearance of 3 years of planting in the field. New growth
symptoms and signs at root collar; death. stops, and foliage wilts and dries on the tree
Unless trees are small, this is usually a slow without becoming chlorotic.
progression. Confirmation of the disease Older trees decline more slowly and may
relies on signs of the pathogen and its isola- linger for 2 years or more before dying.
tion from the host. Mycelial fans are often Affected limbs defoliate and new growth is
found in the cambium of dying or recently stunted and pale green. As foliage becomes
killed trees. Rhizomorphs also form beneath sparser, branches and fruit become increas-
 Diseases of Annonaceae 25

ingly susceptible to sunburn. Flowering and Black canker

fruit set is increased, but fruit are undersized
and non-marketable. Internally, the tree’s This disease, caused by the fungus
vascular system becomes dark brown to Phomopsis annonacearum, is a relatively
black (Plate 3). This symptom may be limited minor problem in Australia (Purss, 1953;
to below the graft union, but usually extends Persley, 1993). It may also occur in
into the canopy. Oozing of the causal bac- California and Florida where Phomopsis sp.
terium from affected woody tissue is evident was reported to cause a fruit spot (Farr et
under the light microscope. In the disease’s al., 1989; Alfieri et al., 1994).
terminal phases, the root collar and sur- Spots on fruit originally are small and
rounding roots rot and disintegrate. purple, and eventually enlarge, crack and
darken to a brown colour (Plate 4) (Cook,
1975). Lesions are superficial (<0.5 cm deep);
Causal agent
their surfaces become hard and embedded
Until 1983, the most probable cause of both with black pycnidia of the fungus. In pycni-
wilt syndromes was assumed to be a species dia, ␣-conidia, 2–3 ⫻ 5–8 ␮m in size, form.
of Phytophthora (Mayers and Hutton, 1987). Infection and disease development are facili-
That year, Ralstonia solanacearum was recov- tated by wet conditions. Since the fungus
ered from root and trunk tissue of an survives on mummified fruit and leaves
affected tree and shown to be pathogenic on beneath trees, these tissues should be
sugar apple and the ‘African Pride’ cultivar removed from the orchard and destroyed.
of atemoya, as well as Casuarina equisetifolia,
potato, pepper and three different cultivars
of tomato. The bacterium is a Gram-nega- Botryodiplodia fruit rot
tive, aerobic rod. The agent is in biovar 3, the
most nutritionally diverse biovar in this This disease has been reported in Australia,
species. It is thought to have originated and Egypt, India, Mauritius and the USA
evolved in Asia (Hayward, 1991). (Florida), and is usually a problem only in
poorly managed orchards (Rao, 1964b;
Lutchmeah, 1988; Snowdon, 1990; Persley,
Epidemiology
1993; Alfieri et al., 1994). Due to the wide
Up to 50% of the trees were killed by this geographic range of the causal agent, the dis-
disease when they were propagated on root- ease may be found in other areas.
stocks of atemoya or sugar apple (Mayers Small purple lesions enlarge and blacken
and Hutton, 1987). The disease occurs most and eventually are covered with black pycni-
commonly in wet areas or those with poorly dia (Plate 5) (Snowdon, 1990; Persley, 1993).
drained soils. Unlike black canker lesions, these penetrate
the flesh that, depending on the presence of
secondary microbes, eventually softens or
Management hardens and cracks. Fruit usually remain
No chemical control measures are available. attached to the tree. The pathogen also
Free-draining soils and pathogen-free plant- causes a blight and dieback of small
ing materials should be used when new branches (Cook, 1975; Farr et al., 1989).
orchards are planted (Persley, 1993). Sugar Botryodiplodia fruit rot is caused by
apple is very susceptible, and its use as a Diplodia theobromae which is described in
rootstock should be avoided wherever there Chapter 1. The disease’s common name
is a threat from this disease (George et al., comes from the genus in which the pathogen
1987). Cherimoya is much less susceptible, formerly was placed. It survives on dead
and some cultivars are more resistant than host tissue, especially mummified fruit. The
others. Alternative host crops of the disease is managed by removing these reser-
pathogen should not be interplanted with voirs of inoculum from orchards and
trees, and weed hosts should be controlled. destroying them.
26 R.C. Ploetz

Cylindrocladium leaf and fruit spot 45–90 ⫻ 4–7 ␮m macroconidia that are held
in parallel clusters by colourless slime.
This disease was described in Queensland, Macroconidiophores consist of a septate
Australia on atemoya and in Brazil on sugar 80–200 ⫻ 6–7 ␮m stipe, penicilliate arrange-
apple (Figueiredo and Namekata, 1967; ment of fertile branches, a septate 120–240 ⫻
Hutton and Sanewski, 1988). It is usually an 3–4 ␮m stipe extension and a narrowly
unimportant disease, but can cause serious clavate 2–3 ␮m diameter vesicle.
fruit losses during periods of heavy rainfall.
Epidemiology
Symptoms
Since the causal fungi are soilborne, damage
Symptoms on leaves and fruit begin as black is most often prevalent in lower portions of
spots 1–2 mm in diameter (Hutton and the canopy (Hutton and Sanewski, 1988). In
Sanewski, 1988). Spots on fruit are skin deep, Australia, the disease has also been observed
not sunken and eventually dry out and crack higher in the canopy as a result of soil that
(Plate 6). As they enlarge, they coalesce to has been transported by the coastal brown
form large, irregular, brownish-black lesions ant, Pheidole megacephala, when building pro-
that may elongate during wet periods down tective tunnels.
the sides of the fruit. The centres of lesions
on leaves become light tan as they enlarge
and coalesce (Plate 7). Stems and roots were
also infected experimentally.

Causal agents
Cylindrocladium colhounii causes Cylindro-
cladium leaf and fruit spot in Queensland
(Hutton and Sanewski, 1988). The fungus’s
teleomorph, Calonectria colhounii, was not
reported. In Brazil, Calonectria leguminum
(anamorph: Cylindrocladium leguminum) causes
the disease (Figueiredo and Namekata, 1967).
C. colhounii produces cylindrical, straight,
two- to four-celled, 45–80 ⫻ 4–6 ␮m macro-
conidia that are held in parallel clusters by a
colourless slime (Fig. 2.1) (Crous, 2002).
Macroconidiophores consist of a septate
80–190 ⫻ 6–7 ␮m stipe, penicilliate arrange-
ment of fertile branches, a septate 160–280 ⫻
3–4 ␮m stipe extension and a clavate 3–4 ␮m
diameter vesicle. Its cardinal temperatures
for growth are >5, <25 and 35°C.
C. leguminum produces orange to red-
brown, subglobose to ovoid perithecia that
are 360–580 ␮m high and 300–440 ␮m in
width (Fig. 2.2) (Crous, 2002). Asci are
clavate, 76–126 ⫻ 13–22 ␮m, taper to a long,
thin stalk, and contain eight ascospores that Fig. 2.1. (A) Macroconidiophore, (B) macroconidia
are hyaline, fusoid with rounded ends, and (C) macrovesicles of Cylindrocladium
slightly curved, two- to four-celled and colhounii, and (D) ascus and ascospores of its
30–100 ⫻ 4–8 ␮m. The anamorph produces teleomorph, Calonectria colhounii. Bar = 10 ␮m
hyaline, cylindrical, two- to seven-celled, (from Crous, 2002).
 Diseases of Annonaceae 27

in the markets of Poona (Rao, 1964a). The

disease usually originated at the stem end of
fruit as purplish brown, irregular spots that
turned brown with age and eventually cov-
ered large areas of the fruit surface. The
affected areas remained firm, and affected
fruit failed to ripen. The causal fungus,
Pestalotia sp., produced fusiform, five-celled
conidia with the three central cells coloured
a deep brown; they were 21–28 ⫻ 8–10 ␮m
and had three or four divergent setulae at
the apex. After artificial inoculation, the fun-
gus affected sugar apple, but not soursop
and fruit of several other species. Based on
its morphology and host range, Rao (1964a)
felt that the fungus was sufficiently different
to be considered a new species.

Phytophthora root and fruit rot (purple blotch)

Phytophthora root and fruit rot have been

reported in Australia, India, Malaysia, the
Philippines, Spain and the USA (California
and Hawaii) (Reinking, 1923; Purss, 1953; Rao
et al., 1962; Chee, 1969; Gomez, 1983; French,
1987; Persley, 1993; Tsao et al., 1994; J.Y.
Uchida, University of Hawaii, personal com-
munication). Based on the wide host ranges of
Fig. 2.2. (A) Macroconidiophores, (B) macrovesicles its causal agents, it probably occurs in other
and (C) macroconidia of Cylindrocladium leguminum, locations in which these pathogens are found.
and (D) ascospores of its teleomorph, Calonectria
leguminum. Bar = 10 ␮m (from Crous, 2002).
Symptoms
Aboveground symptoms appear first on
Management
immature fruit as small, water-soaked
Low-lying branches should be removed to lesions, especially on fruit that are near the
avoid fruit and foliage contact with soil and soil surface. Affected fruit abscise, and exces-
increase air circulation. Mulch under trees sive losses of all ages of fruit can occur. As
and permanent sod in the middles will symptoms progress, they become purplish to
reduce dispersal of inoculum, as will the black, extend over large areas of the fruit
control of ants and the mealybugs that they surface, and extend as a brownish decay into
service. Of two popular cultivars of atemoya the fruit pulp (Plate 8). Fruits eventually
in Australia, ‘Pinks Mammoth’ was less sus- harden and mummify, the fruit interior rots
ceptible than ‘African Pride’. completely and the seeds shrivel. The causal
agents are soilborne and also cause dark-
coloured root decay.
Pestalotia fruit spot
Causal agents
Pestalotia fruit spot is a minor disease of
sugar apple. It was reported in India where it Phytophthora palmivora is the primary cause
was observed at low levels (3–5% incidence) of Phytophthora root and fruit rot
28 R.C. Ploetz

(Reinking, 1923; Purss, 1953; Chee, 1969; from herbaceous hosts), no or poor growth
Tsao et al., 1994). It affects atemoya, pond at 35°C, weak or no virulence on Capsicum,
apple, soursop and sugar apple. P. nicotianae and distinct isozyme and mitochondrial
has been reported on sugar apple in India DNA profiles (Aragaki and Uchida, 2001).
(Rao et al., 1962), and P. cinnamomi causes a The above species can be distinguished
root and collar rot on cherimoya in Spain by the following sporangial characteristics.
(Gomez, 1983). Phytophthora sp. has been Those of P. palmivora, P. tropicalis and P. cap-
reported on sugar apple in California sici are papillate and caducous, but the
(French, 1987). pedicels of P. palmivora are usually ~10
Recent reports have indicted two addi- times shorter than those of P. tropicalis and
tional species. Weinert et al. (1998) reported P. capsici (5 versus 50 ␮m or more). P. tropi-
that an isolate from sugar apple in calis produces sporangia that have a pre-
Queensland that had been identified as P. dominantly tapered base and are narrower
palmivora (UQ3691) was actually P. capsici. (≤26 ␮m in diameter) and have a greater
Aragaki and Uchida (2001) examined 100 length : breadth ratio (≥1.8) than P. capsici
isolates from herbaceous and woody hosts (Fig. 2.4). Sporangia of P. cinnamomi and P.
that included A. cherimola from the islands nicotianae are non-caducous but, unlike
of Hawaii and Oahu; based on the broad those of P. cinnamomi, those of P. nicotianae
concept of the species (Erwin and Ribiero, are papillate.
1996), all were considered P. capsici. Based
on molecular data from others and mor-
phological and pathological data of their
own, Aragaki and Uchida (2001) proposed
that the isolates from woody hosts com-
prised a distinct taxon that they named P.
tropicalis. How widespread P. tropicalis is on
annonas and whether diseases that previ-
ously were attributed to either P. capsici or
P. palmivora were actually caused by it is
not known.
Features of P. cinnamomi, P. nicotianae and
P. palmivora are found in Chapter 1. In the
broad sense, P. capsici possesses the follow-
ing traits (Erwin and Ribiero, 1996). It pro-
duces ovoid to ellipsoid, papillate to
semipapillate, caducous sporangia that have
long pedicels (Fig. 2.3). Some sporangia
have more than one papillum. Average
dimensions of the UQ3691 strain from sugar
apple were 40 ⫻ 24 ␮m with pedicels that
exceeded 50 ␮m in length. P. capsici is het-
erothallic. Oogonia are 23–50 ␮m in diame-
ter and spherical or subspherical, and
antheridia are amphigynous. Oospores are
usually plerotic with cell walls between 2
Fig. 2.3. Variable sporangia of Phytophthora
and 6 ␮m thick. Its cardinal temperatures for
capsici. Clockwise from the upper right: ellipsoid,
growth are 10, 28 and >35°C. P. tropicalis was bilaterally asymmetrical, bipapillate, ellipsoid with
distinguished from P. capsici by its produc- tapered base, nearly spherical, intercalary
tion of chlamydospores by most isolates deciduous, and typical sporangia from pepper. Bars
(27–33 ␮m in diameter; chlamydospores are = 40 ␮m except for the first micrograph where it is
generally not formed by strains of P. capsici 25 ␮m (from Aragaki and Uchida, 2001).
 Diseases of Annonaceae 29

Epidemiology
All of the above species have wide host
ranges. Erwin and Ribiero (1996) reported
~200 hosts for P. palmivora, and Reinking
(1923) demonstrated that isolates from
coconut palm and cacao both caused severe
disease on seedlings of soursop. Erwin and
Ribiero (1996) listed more than 300 hosts
for P. nicotianae, and Rao et al. (1962)
showed that isolates from sugar apple
caused either fruit or root rots on ~20 dif-
ferent species.
Rainfall favours disease development.
Fruit usually abscise within 4 days of the
appearance of purple lesions.

Management
Low-lying branches in the canopy should
be removed. Mulches can reduce disease on
fruit by reducing rainsplash dispersal of
inoculum. Grass or other living mulches
should be maintained between rows.
Fungicidal control has not been reported.

Pink disease

The disease is not common, and appears

during wet weather in mainly tropical areas
(Persley, 1993). The causal fungus,
Erythricium salmonicolor, has a wide host
range and is described in Chapter 1. It forms
light pink mats of mycelium on trunk and
branch surfaces (Plate 9). Eventually, affected
bark cracks and oozes gum. Affected areas
should be pruned from trees and treated
with a fungicide.

Pseudocercospora fruit and leaf spot

This disease is caused by a non-described

species of Pseudocercospora, and may be
widely distributed. It is a serious problem in
Fig. 2.4. Sporangia of Phytophthora tropicalis.
Queensland where up to 50% of the fruit in a
Clockwise from the top: typical sporangia from given orchard may be affected (Persley, 1993;
anthurium, ellipsoid with tapered base, bilaterally although the affected taxa were not reported
asymmetrical, ellipsoid and pyriform. Note the in this publication, symptoms of the disease
tapered base of most of these sporangia. Bar = were shown on custard apple). A leafspot
40 ␮m (from Aragaki and Uchida, 2001). caused by Pseudocercospora sp. has been
30 R.C. Ploetz

reported on pond apple in Florida (Alfieri et Pythium splendens causes the disease in
al., 1994), and there are numerous old reports Florida (Ploetz, 1991), and is described in
of species of Cercospora causing damage on detail in Chapter 6. Pythium sp. has been
custard apple and sugar apple in Brazil (C. reported in California (Farr et al., 1989).
anacardii and C. anonae) and India (C. anonae This disease most often starts in the nurs-
and C. caracasensis) (Muller and Chupp, 1935; ery when contaminated soil or potting mix is
Mundkur and Ahmad, 1946; Holliday, 1980). used or where plants are placed on the
Since the latter reports were published ground. Clean pots and media should be
before Pseudocercospora was widely recog- used whenever possible. Metalaxyl was
nized as a distinct segregate of Cercospora, it effective in pot studies, but its performance
is possible that all of the above diseases are in the field has not been documented (Ploetz,
caused by a single pathogen or closely unpublished results).
related pathogens.
Symptoms begin in natural crevices on the
fruit surface as purple-grey spots, 1–5 mm in Rust
diameter (Persley, 1993). Spots coalesce,
increase to 10–15 mm in diameter, and Cummins (1941) reported that this disease
darken with age (Plate 10). Badly affected was common from Florida to Ecuador. It
fruit may crack, and be badly disfigured and affects atemoya, cherimoya, custard apple,
unmarketable. On leaves, irregular dark red ilama and sugar apple, and can cause con-
to brown lesions, 1–5 mm in diameter, form siderable defoliation in summer and
on the adaxial surface. The causal fungus autumn. However, specific control measures
eventually sporulates in necrotic areas in the are usually not indicated.
centre of these lesions. The causal fungus, Phakopsora cherimoliae,
The pathogen’s large conidia are dissemi- produces telia in the base of old uredia or in
nated by wind, and infection requires free separate subepidermal reddish brown crusts,
moisture. Affected fruits from the previous 0.1–1 mm in diameter and 3–6 spores in thick-
season should be removed from the orchard
before fruit set in the current season begins.
Fungicides should be applied at the onset of
fruit set.

Pythium root rot

Although this disease has only been reported

in California and Florida, it can be quite
damaging. Atemoya, cherimoya, custard
apple and sugar apple are affected (Farr et
al., 1989; Ploetz, 1991; Alfieri et al., 1994).
Aboveground symptoms include a thin,
often chlorotic canopy and a general reduc-
tion in tree size and vigour (Fig. 2.5).
Although damage is usually most severe in
low-lying or poorly drained areas in a field,
healthy trees may surround affected indi-
viduals. The cortical tissues of roots are
brown and can be easily removed from the
stele. When aboveground symptoms are Fig. 2.5. Aboveground symptoms of Pythium root rot,
evident, root systems are often so severely caused by Pythium splendens, on a ‘Gefner’ atemoya
rotted that trees can be removed from the tree. Note the chlorotic, sparse canopy and the
soil by hand. healthy tree in the background (photo: R.C. Ploetz).
 Diseases of Annonaceae 31

ness. Teliospores, the outer layers of which minor problem on soursop in the state of
are golden or chestnut-brown, are cubical, Ceara. Affected leaves display vein clearing
oblong or oblong–ellipsoid and 7–13 ␮m ⫻ and diffuse, chlorotic areas that may be asso-
13–23 ␮m. Their cell walls are 1–2 ␮m thick. ciated with some distortion of the laminar
surface. Artificially inoculated seedlings
were stunted, but rarely died. The authors
Scab felt that yield losses could occur if plants
were infected at an early age.
This disease was reported in Brazil and A rhabdovirus was observed in field and
Venezuela on cherimoya and sugar apple experimentally infected plants (Katijima et
(Bitancourt and Jenkins, 1942). Dark spots al., 1993). In leaf-dip preparations, it mea-
with brown margins form on leaves and may sured 60–70 nm ⫻ 250–300 nm and con-
coalesce into large irregular patches. They tained a 40–50 nm wide inner component
are less noticeable on the abaxial surface, and with a transverse periodicity of 5 nm. In
their centres eventually lighten and dry out. transmission electron micrographs of leaf
Ascocarps of the causal fungus, Elsinoë thin sections, the virus was observed to accu-
annonae, develop in lesion centres. They are mulate in the endoplasmic reticulum, indi-
30–50 ⫻ 50–150 ␮m in diameter, and irregu- cating that it belonged in the type I class of
lar, dark and erumpent. They contain spheri- rhabdoviruses.
cal asci, 20 ␮m in diameter, which in turn The virus was transmitted mechanically
contain eight hyaline, three-celled ascospores to seedlings of soursop, but not to biriba and
that are 5–8 ⫻ 12–15 ␮m. Acervuli of the sugar apple. It was transmitted most effec-
anamorph, which presumably is a species of tively to soursop via grafting, and could also
Sphaceloma, may form in old lesions. be transmitted to biriba and sugar apple in
this manner, although the virus did not
appear to move beyond the graft regions in
Yellow blotch the latter plants. Spread of the disease in the
field suggested that an unidentified insect
Yellow blotch was reported in Brazil vector transmitted the virus. No control mea-
(Katijima et al., 1993). It appears to be a sures were indicated.

Table 2.1. Miscellaneous minor diseases of fruit crops in the Annonaceae.

Affected
Disease taxaa Cause(s) Reference(s)

Cherimoya cambium disease ch Ascochyta cherimolae Garmedia (1945)

Fruit rot sa Botrytis sp. Alfieri et al. (1994)
sa Phylctema sp. Alfieri et al. (1994)
Gliocladium rot sa Gliocladium roseum Chaudry et al. (1985)
Leaf necrosis il Corynespora sp. Alfieri et al. (1994)
Leaf spot sa Alternaria alternata Kamal and Chandra (1980)
ns, sa Alternaria sp. Farr et al. (1989); Alfieri et
al. (1994)
ns, pa Diplodia sp. Alfieri et al. (1994)
ca, ch, ns, sa, pa Gloeosporium sp. Alfieri et al. (1994)
sa Helminthosporium sp. Alfieri et al. (1994)
sa Mycosphaerella sp. Farr et al. (1989)
so Phyllostictina anonicola Batista (1952)
ca, ch, ns, sa Phyllosticta sp. Alfieri et al. (1994)
ns Stemphylium sp. Alfieri et al. (1994)

Continued
32 R.C. Ploetz

Table 2.1. Continued.

Affected
Disease taxaa Cause(s) Reference(s)

Not specified ch Dothiorella sp. Farr et al. (1989)

ch Penicillium sp. Farr et al. (1989)
so Phyllachora anonicola Chardon et al. (1940)
ch Phytomonas sp. Fernández-Becerra et al.
(1996)
ch Rhizoctonia solani Farr et al. (1989)
ch Verticillium dahliae Farr et al. (1989)
Pink mould rot sa Trichothecium roseum Chaudry et al. (1985)
Root rot sa Phymatotrichopsis
omnivora Farr et al. (1989)
ch Rosellinia necatrix Montemartini (1934)
aat = atemoya, A. cherimola ⫻ A. squamosa; ca = custard apple or Bullock’s heart, A. reticulata L.;
ch = cherimoya, A. cherimola Mill.; il = ilama, A. diversifolia Saff.; ns = not specified; pa = pond apple,
A. glabra L.; so = soursop, A. muricata L.; sa = sugar apple or sweetsop, A. squamosa L.

References

Abo-El-Dahab, M.K. and El-Goorani, M.A. (1971) Market and storage diseases of Annona squamosa L.
fruits in U.A.R. (Egypt). Phytopatologia Mediterranea 10, 107–109.
Alfieri, S.A., Jr, Langdon, K.R., Kimbrough, J.W., El-Gholl, N.E. and Wehlburg, C. (1994) Diseases and
Disorders of Plants in Florida. Bulletin No. 14, Florida Department of Agriculture and Consumer
Services, Contribution No. 680.
Alvarez-García, L.A. (1949) Anthracnose of the Annonaceae in Puerto Rico. Journal of Agriculture
University of Puerto Rico 33, 27–43.
Aragaki, M. and Uchida, J.Y. (2001) Morphological distinctions between Phytophthora capsici and P. tropi-
calis sp. nov. Mycologia 93, 137–145.
Aruda, S.C. (1940) Antracnose e cancro das Anonaceas. Biologico 6, 224–225.
Batista, A.C. (1952) Algumas novas espécies de Phyllosticta e Phyllostictina. Boletin da Secretaria da
Agricultura da Pernambuco 19, 3–4.
Batista, A.C. (1953) Novos fungos agents de antracnose. Annual Congress of the Society of Botany Brasil.
pp. 142–144.
Bitancourt, A.A. and Jenkins, A.E. (1942) New discoveries of Myriangiales in the Americas. Proceedings of
the Eighth American Science Conference 1940, 3, 149–172.
Brown, B.I., Wong, L.S., George, A.P. and Nissen, R.J. (1988) Comparative studies on the postharvest
physiology of fruit from different species of Annona (custard apple). Journal of Horticultural Science
63, 521–528.
Chardon, C.E., Miller, J.H. and Miller, A.S. (1940) Ascomycetes from the state of Minas Geraes (Brazil).
Mycologia 32, 172–204.
Chaudry, A.S., Singh, G.N. and Singh, A.R. (1985) Effect of wrapping materials and ripening media on
physico-chemical compositions of custard apple (Annona squamosa Linn.). Indian Journal of
Agricultural Research 19, 90–92.
Chee, K.H. (1969) Hosts of Phytophthora palmivora. Review of Applied Mycology 48, 337–344.
Ciferri, R. and González-Fragoso, R. (1927) Hongos parásiticos y saprofitos de la República Dominicana.
(9th Serie.). Boletin Real Sociedad Española Histologia 27, 68–81.
Cook, A.A. (1975) Diseases of Tropical and Subtropical Fruits and Nuts. Hafner Press. New York.
Crous, P.W. (2002) Taxonomy and Pathology of Cylindrocladium (Calonectria) and Allied Genera. APS Press,
St Paul, Minnesota.
Cummins, G.B. (1941) Descriptions of tropical rusts. IV. Bulletin of the Torrey Botanical Club 68, 467–472.
DeCarvalho, T. (1948) Relacão preliminary de doenas encontradas em plantes e insectos com anatações
fitopatológicas. Colónia de Moçambique, Repartição de Agricultura, Seccão de Micologia.
 Diseases of Annonaceae 33

Deighton, F.C. (1939) Mycological Work. Report of the Department of Agriculture Sierra Leone, 1938,
pp. 64–66.
Erwin, D.C. and Ribiero, O.K. (1996) Phytophthora Diseases Worldwide. APS Press, St Paul, Minnesota.
Farr, D.F., Bills, G.F., Chamuris, G.P. and Rossman, A.Y. (1989) Fungi on Plant and Plant Products in the
United States. APS Press, St Paul, Minnesota.
Fernández-Becerra, C., Osuna, A., Muller, E., Dollet, M. and Sánche-Moreno, M. (1996) Characterization
of Phytomonas isolated from fruits by electrophoretic isoenzymes and kinetoplast DNA analysis.
FEMS Microbiology Letters 145, 463–468.
Figueiredo, M.B. and Namekata, T. (1967) Constatação de Calonectria quinqueseptata n.sp., forma perfeita
de Cylindrocladium quinqueseptata Boedijn and Reitsma, sôbre Anonna squamosa L. e Eucalyptus sp.
Arquivos do Instituto Biologico, São Paolo 34, 91–96.
French, A.M. (1987) California Plant Disease Host Index. Part 1: Fruit and Nuts. California Department of
Food and Agriculture.
Garmendia, J.O. (1945) La enfermedad del cambium en chirimoyos. Simiente 14, 38.
George, A.P., Nissen, R.J. and Brown, B.I. (1987) The custard apple. Queensland Agricultural Journal
287–296.
Gomez, M.C. (1983) The cherimoya. In: Chambers, C.M. (ed.) California Rare Fruit Growers Yearbook 15, 5–29.
Hayward, A.C. (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum.
Annual Review of Phytopathology 29, 65–87.
Holliday, P. (1980) Fungus Diseases of Tropical Crops. Cambridge University Press. Cambridge, UK.
Hutton, D.G. and Sanewski, G.M. (1988) Cylindrocladium leaf and fruit spot of custard apple in
Queensland. Australasian Plant Pathology 18, 15–16.
Kamal, and Chandra, G. (1980) On sclerotial rot of Nigelia sativa and Alternaria leaf spot of Annona
squamosa – new to India. Indian Journal of Mycology and Plant Pathology 9, 88.
Katijima, E.W., Martins, C.R.F. and Santos, A.A. (1993) Identification of a rhabdovirus in soursop (Annona
muricata). Plant Disease 77, 276–278.
Kile, G.A, Guillaumin, J.J., Mohammed, C. and Watling, R. (1994) Biogeography and pathology of
Armillaria. In: Johanson, M. and Stenlind, J. (eds) Proceedings of the Eighth International Conference on
Root and Butt Rots. IUFRO, Uppsala, pp. 411–436.
Li, L.Y. (1936) Anthracnose of Hwangpee, Clausena lansium (Lour.) Skeels, in South China. Lingnan Science
Journal 15, 113–117.
Lutchmeah, R.S. (1988) Botryodiplodia theobromae causing fruit rot of Annona squamosa in Mauritius. Plant
Pathology 37, 152.
Martin, F.W., Campbell, C.W. and Ruberté, R.M. (1987) Perennial Edible Fruits of the Tropics: an Inventory.
Agriculture Handbook No. 642, US Department of Agriculture, Washington, DC.
Mayers, P.E. and Hutton, D.G. (1987) Bacterial wilt, a new disease of custard apple: symptoms and etiol-
ogy. Annals of Applied Biology 111, 135–141.
Montemartini, L. (1934) I parassiti e le malattie delle piante coltivate nella Sicilia occidentale durante il
biennio 1932–33. Rivista di Patologia Vegetale 24, 11–36.
Muller, A.S. and Chupp, C. (1935) Cercosporae de Minas Geraes. Arquives da Instituto da Biologia Vegetal 1,
213–220.
Mundkur, B.B. and Ahmad, S. (1946) Revisions of and additions to Indian fungi. II. Mycological Papers,
Imperial Mycological Institute 18.
Mwenje, E. and Ride, J.P. (1997) The use of pectic enzymes in the characterization of Armillaria isolates
from Africa. Plant Pathology 46, 341–354.
Nakasone, H.Y. and Paull, R.E. (1998) Tropical Fruits. CAB International, Wallingford, UK.
Núñez-Elisea, R., Schaffer, B., Fisher, J.B., Colls, A.M. and Crane, J.H. (1999) Influence of flooding on net
CO2 assimilation, growth and stem anatomy of Annona species. Annals of Botany 84, 771–780.
Paull, R.E. (1996) Postharvest atemoya fruit splitting during ripening. Postharvest Biology and Technology 8,
329–334.
Persley, D. (ed.) (1993) Diseases of Fruit Crops. Department of Primary Industries, Brisbane.
Ploetz, R.C. (1991) Species of Pythium as pathogens of perennial, woody fruit crops in south Florida
(Abstract). Phytopathology 81, 699.
Purss, G.S. (1953) The fruit rots of the custard apple. Queensland Journal of Agricultural Science 10, 247–265.
Raabe, R.D., Conners, I.L. and Martinez, A.P. (1981) Checklist of Plant Diseases in Hawaii. Information Text
Series no. 22. Hawaii Institute of Tropical Agriculture and Human Resources, College of Tropical
Agriculture and Human Resources, University of Hawaii.
34 R.C. Ploetz

Rao, V.G. (1964a) A new fruit spot of Annona squamosa from India. Plant Disease Reporter 48, 399–401.
Rao, V.G. (1964b) Some new market and storage diseases of fruits and vegetables in Bombay-
Maharashtra. Mycopathologia et Mycologia Applicata 23, 297–310.
Rao, V.G., Desai, M.K. and Kulkarni, N.B. (1962) A new Phytophthora fruit rot of Annona squamosa from
India. Plant Disease Reporter 46, 874–876.
Reinking, O.A. (1923) Comparative study of Phytophthora faberi on coconut and cacao in the Philippine
Islands. Journal of Agricultural Research 25, 267–284.
Rhoads, A.S. (1942) Notes on Clitocybe root rot of bananas and other plants in Florida. Phytopathology 32,
487–496.
Shaw, C.G., III and Kile, G.A. (1991) Armillaria Root Disease. Agricultural Handbook No. 691. Forest
Service, US Department of Agriculture, Washington, DC.
Small, W. (1926) Report of the mycologist for the period January 1st to September 30th. Annual Report of
the Ugandan Department of Agriculture for the Year Ended 31st December, 1925.
Snowden, J.D. (1921) Report of the Government Botanist for the period 1st April to 31st December, 1920.
Annual Report for the Department of Agriculture, 1920, pp. 43–46.
Snowdon, A.L. (1990) A Colour Atlas of Post-harvest Diseases and Disorders of Fruits and Vegetables. Vol. 1:
General Introduction and Fruits. Wolfe Scientific, London.
Tsao, P.H., Gruber, L.C., Potales, L.A., Gochangco, A.M., Luzaran, P.B., de los Santos, A.B. and Pag, H.
(1994) Some new records of Phytophthora crown and root rots in the Philippines and in world liter-
ature. (Abstract) Phytopathology 84, 871.
Vock, N.T. (1978) A Handbook of Plant Diseases, Vol. 1. Queensland Department of Primary Industries,
Brisbane.
Weinert, M.P., Smith, B.N., Wagels, G., Hutton, D. and Drenth, A. (1998) First record of Phytophthora cap-
sici from Queensland. Australasian Plant Pathology 28, 93.