Skip to main content
SpringerLink
Log in

Reproductive ecology of white cacao (Theobroma bicolor Humb. & Bonpl.) in Ecuador, western Amazonia: floral visitors and the impact of fungus and mistletoe on fruit production

  • Ecology & Biogeography - Original Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

Theobroma bicolor is widely distributed in the Neotropics with great potential for economic use. However, very little is available in literature about its pollinators and reproductive ecology in comparison to what is available about its economically more important relative T. cacao. We studied aspects of the floral biology, reproductive phenology and biotic restrictions to the reproduction of the species. We measured, observed and monitored flowers and described their morphology, breeding system, receptivity times of the stigma and peaks of flower and fruit production. During 20 consecutive days, we collected floral visitors of 135 ± 45 flowers per day. We also calculated the damage in fruit production generated by the mistletoe (Oryctanthus cf. alveolatus) and the fungus (Moniliophthora roreri). We found that flower stigma was more receptive between 6:00–10:00 and flowers last up to three days on the tree, which is less time than what has been reported elsewhere. We collected 211 insects from 68 different morphotypes, but five of these represented 49.8% of the total; specimens of Ceratopogonidae, Chironimidae and Sciaridae were the most abundant and could be pollinators of the species. The flowering of T. bicolor showed a positive correlation (r > 0.75) with the months with higher temperature and solar radiation. We recorded an average per tree of 7 ± 5 fruits. We found a drastic loss of 84% of fruits in the plants infested by the mistletoe O. cf. alveolatus and of 29% when infested by the fungus M. roreri. The results of this study serve as a basis to generate local management practices.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adjaloo MK, Oduro W, Banful BK (2012) Floral phenology of upper amazon cocoa trees: implications for reproduction and productivity of cocoa. ISRN Agron 2012:1–8. https://doi.org/10.5402/2012/461674

    Article  Google Scholar 

  • Aikpokpodion P (2012) Phenology of flowering in cacao (Theobroma cacao) and its related species in Nigeria. Afr J Agric Res 7:3395–3402. https://doi.org/10.5897/ajar11.1608

    Article  Google Scholar 

  • Alvarado A, Carrera M, Morante J (2018) Importancia de la MosquillaForcipomyia Spp. en la Polinización y Producción de Cultivo de Cacao. Rev DELOS Desarro Local Sosten 11:20

    Google Scholar 

  • Arenas-De-Souza MD, Rossi A, Varella T et al (2016) Receptividadestigmatica e viabilidadpolínicaem Theobroma subincanum Mart : Especiefrutífera da regiãoamazónica. Rev Bras Frutic. https://doi.org/10.1590/0100-29452016757

    Article  Google Scholar 

  • Barrera JA, Hernández MS, Vargas G et al (2006) Caracterización del crecimiento y desarrollo vegetativo de especies promisorias del género Theobroma bajo condiciones de la Amazonia colombiana. Theobroma, 1st edn. Bogotá, Colombia, pp 65–100

    Google Scholar 

  • Bruni R, Bianchini E, Bettarello L et al (2000) Lipid composition of wild Ecuadorian Theobroma subincanum Mart. seeds and comparison with two varieties of Theobroma cacao L. J Agric Food Chem 48:691–694. https://doi.org/10.1021/jf991015n

    Article  CAS  PubMed  Google Scholar 

  • Calzavara BBG, Müller CH, Kahwage ONC (1984) Tropical fruticulture: copuassu. Cultivation, processing and fruit. EMBRAPA/CPATU, Belém, Brazil, p 101

    Google Scholar 

  • Claus G, Vanhove W, Van Damme P, Smagghe G (2018) Challenges in cocoa pollination: the case of Côte d’Ivoire. Pollinat Plants. https://doi.org/10.5772/intechopen.75361

    Article  Google Scholar 

  • Cuatrecasas J (1964) Cacao and its Allies A taxonomic revision of the genus Theobroma. Natl Herb 35:379–607

    Google Scholar 

  • Cuéllar AS, Daza MAH, León CHR et al (2015) Reacción a Moniliophthora roreri en Theobroma spp. en Caquetá. Colombia Summa Phytopathol 41:183–190. https://doi.org/10.1590/0100-5405/2026

    Article  Google Scholar 

  • Dafni A (1992) Stigma receptivity. Pollination ecology a practical approcach. Oxford University Press, New York, pp 78–82

    Google Scholar 

  • Dafni A, Firmage D (2000) Pollen viability and longevity: Practical, ecological and evolutionary implications. Plant Syst Evol 222:113–132. https://doi.org/10.1007/BF00984098

    Article  Google Scholar 

  • De Souza MS, Venturieri GA (2010) Floral biology of cacauhy (Theobroma speciosum, Malvaceae). Brazilian Arch Biol Technol 53:861–872. https://doi.org/10.1590/s1516-89132010000400016

    Article  Google Scholar 

  • Dueñas-Gómez H (2001) Sinopsis de las Loranthaceae de Colombia. Caldasia 23:81–99

    Google Scholar 

  • Esteves PR, Magalhães M, Amaral F et al (2009) Performance polínica em cacaueiros (Theobroma cacao L.) autocompatíveis e autoincompatíveis. Rev Bras Bot 32:617–620. https://doi.org/10.1590/s0100-84042009000300019

    Article  Google Scholar 

  • Evans HC (1978) Witches’ broom disease of cocoa (Crinipellis perniciosa) in Ecuador. Ann Appl Biol 89:185–192. https://doi.org/10.1111/j.1744-7348.1978.tb07689.x

    Article  Google Scholar 

  • FDA (2020) Daily value and percent daily value: changes on the new nutrition and supplement facts labels. https://www.fda.gov

  • Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315. https://doi.org/10.1002/joc.5086

    Article  Google Scholar 

  • Forbes S, Northfield T (2016) Increased pollinator habitat enhance cacao fruit set and predator conservation. Ecol Appl 27:887–899. https://doi.org/10.1002/eap.1491

    Article  Google Scholar 

  • Gálvez-Marroquín L, Reyes-Reyes A, Avendaño-Arrazate C et al (2016) Pataxte (Theobroma bicolor Humb. & Bonpl.): Especie subutilizada en México. Agroproductividad 9:41–47

    Google Scholar 

  • Gan X, Cao L, Zhang X et al (2013) Floral biology, breeding system and pollination ecology of an endangered tree Tetracentron sinense Oliv. (Trochodendraceae). Bot Stud 54:1–9. https://doi.org/10.1186/1999-3110-54-50

    Article  Google Scholar 

  • GBIF (2020) Theobroma bicolor Humb. & Bonpl. Global biodiversity information facility doi: https://doi.org/10.15468/dl.vjk22s%0A. Accessed 12 June 2019

  • Ghersa C (2013) Agroecological basis for managing biotic constraints. In: Christou P, Savin R, Costa-Pierce BA, Misztal I, Whitelaw B (eds) Sustainable Food Production. New York. https://link.springer.com/referencework/https://doi.org/10.1007/978-1-4614-5797-8

  • Gonzáles A, Torres G (2010) Manual Cultivo de Macambo, 1st edn. IIAP, Perú

    Google Scholar 

  • Guerrero NR, Quintero MAO, Naranjo JCP (2012) Determinación del Área Foliar en Fotografías Tomadas con una Cámara Web, un Teléfono Celular o una Cámara Semiprofesional. Rev Fac Nac Agron 65:6399–6405

    Google Scholar 

  • Hernández MS, Casas AE, Martínez O, Galvis JA (1995) Análisis y estimación de parámetros e índices de crecimiento del árbol de maraco (Theobroma bicolorH. BK) a primerafloración. AgronomíaColombiana 12:182–191

    Google Scholar 

  • INC (2016) Nuts and dried fruits, global statistical review, 2015/2016. Int Nut Dried Fruit Counc Found 1–179

  • Jones GD (2012) Pollen analyses for pollination research, unacetolyzed pollen. J Pollinat Ecol 9:96–107. https://doi.org/10.26786/1920-7603(2012)15

    Article  Google Scholar 

  • Kufer J, McNeil C (2006) The jaguar tree (Theobroma bicolor Bompl.) a cultural history of Cacao. In: Chocolate in Mesoamerica, Cameron Mc. University Press of Florida, Gainesville, pp 90–104

  • Leandro M (2017) Biology and epidemiology of Moniliophthora roreri, causal agent of Moniliophthora pod rot of cacao. Tropical agricultural research and higher education center. https://agritrop.cirad.fr/585933/1/Mariela%20Leandro%20PhD%20Thesis.pdf. Accessed 25 November 2019

  • Mantilla L, Piñeres R, Fonseca D (2008) Colombia Frutas de la amazonia. Instituto Sinchi, Bogotá, Colombia

    Google Scholar 

  • Montero-Cedeño SL, Sánchez P, Solórzano R, Pinargote-Borrero AP, Cañarte-Bermúdez EG (2019). Floración y diversidad de insectos polinizadores en un sistema monocultivo de cacao. Revista ESPAMCIENCIA ISSN 1390–8103, 10 (1), 1–7. http://190.15.136.171:4871/index.php/Revista_ESPAMCIENCIA/article/view/178/183

  • Muñoz G-V, Garwood N, Bass M et al (2016) Arboles comunes de Yasuní. Pontificia Universidad Católica del Ecuador, Quito, Ecuador

    Google Scholar 

  • O’Doherty D, Zoll J (2012) Forcipomyia hardyi (Diptera: Ceratopogonidae), a potential pollinator of cacao (Theobroma cacao) flowers in Hawaii. Proceed Hawaiian EntomolSoc 44:79–81

    Google Scholar 

  • Otzoy M (2012) Evaluación de la variabilidad y preservación de parientes silvestres de cacao (Theobroma bicolor y Theobroma angustifolium) provenientes de la región suroccidental de Guatemala. Guatemala

  • Peñuela-Mora M, Schwarz A, Monteros A et al (2016) Guía de la Agrobiodiversidad Tres comunidades kichwa: Atacapi. Universidad Regional Amazónica Ikiam, Quito, Ecuador, Alto Tena y Pumayacu

    Google Scholar 

  • Peterson R, Slovin JP, Chen C (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol 1:66–69. https://doi.org/10.4081/pb.2010.e13

    Article  Google Scholar 

  • Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plan Physiol 27:595–607

    CAS  Google Scholar 

  • Press M, Scholes J, Watling J (2002) Parasitic plants: physiological and ecological interactions with their hosts. In: Physiological Plant Ecology: 39th Symposium of the British Ecological Society. Cambridge University Press, p 175

  • Pugliese AG, Tomas-Barberan FA, Truchado P et al (2013) Flavonoids, proanthocyanidins, vitamin C, and antioxidant activity of Theobroma grandiflorum (Cupuassu) pulp and seeds. J Agric Food Chem 61:2720–2728. https://doi.org/10.1021/jf304349u

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing

  • Richardson JE, Whitlock BA, Meerow AW et al (2015) The age of chocolate: a diversification history of Theobroma and Malvaceae. Front Ecol Evol 3:1–14. https://doi.org/10.3389/fevo.2015.00120

    Article  Google Scholar 

  • Rondón JB, Campos L (2005) Revisión taxonómica del género Theobroma (Sterculiaceae) en Venezuela. Acta Botánica Venez 28:113–133

    Google Scholar 

  • Sandoval C (2017) Conocimiento ecológico tradicional asociado a la elaboración del Siaab g’ez, bebida tradicional de la comunidad zapoteca de Teotitlán del Valle, Oaxaca. Universidad Politécnica de Cataluña Barcelonatech, México

    Google Scholar 

  • Santos RC, Pires JL, Correa RX (2012) Morphological characterization of leaf, flower, fruit and seed traits among Brazilian Theobroma L. species. Genet Resour Crop Evol 59:327–345. https://doi.org/10.1007/s10722-011-9685-6

    Article  Google Scholar 

  • Shivanna K, Sawhney V (1997) Pollen biotechnology for crop production and improvement. Cambridge University Press, New York

    Book  Google Scholar 

  • Sifuentes M (2017) Evaluación físico-química de la pulpa y semilla de dos morfotipos del fruto de macambo “Theobroma bicolor (Humb. & Bompl.)”de la región Loreto, 2015. Universidad Nacional de la Amazonia Peruana

  • Smitha GR, Thondaiman V. (2016) Reproductive biology and breeding system of Saraca asoca (Roxb.) De Wilde: a vulnerable medicinal plant. Springer plus 5:2095 Doi: https://doi.org/10.1186/s40064-016-3709-9

  • Soria D (1974) Indução da produção emcacaueiro com uso de atomizadormotorizadoportátilna Bahia, Brasil Rev. Theobroma 4:3–13. https://doi.org/10.1017/CBO9781107415324.004

    Article  Google Scholar 

  • Srinivasnaik S, Suganthy M, Jegadeeswari V, Mohan Kumar S (2015) Seasonal abundance of major sucking pests of cocoa. In III International Symposium on Underutilized Plant Species Doi: https://doi.org/10.17660/ActaHortic.2019.1241.78

  • Toledo-Hernández M, Wanger TC, Tscharntke T (2017) Neglected pollinators: can enhanced pollination services improve cocoa yields? a review. AgrEcosyst Environ 247:137–148

    Article  Google Scholar 

  • Venegas F, Muñoz R (1984) Malezas tropicales del litoral ecuatoriano. Quevedo, Ecuador

    Google Scholar 

  • Venturieri GA (2011) Flowering levels, harvest season and yields of cupuassu (Theobroma grandiflorum). Acta Amaz 41:143–152. https://doi.org/10.1590/s0044-59672011000100017

    Article  Google Scholar 

  • Vera-Chang J, Cabrera-Verdezoto R, Morán-Morán J et al (2016) Evaluación de tres métodos de polinización artificial en clones de cacao (Theobroma cacao L.) CCN-51 Evaluation of three methods of artificial pollination in clones. Idesia 34:35–40. https://doi.org/10.4067/S0718-34292016005000033.36

    Article  Google Scholar 

  • Wetzstein HY, Yi W, Porter JA, Ravid N (2013) Flower position and size impact ovule number per flower, fruit set, and fruit size in pomegranate. J Am Soc Hortic Sci 138:159–166. https://doi.org/10.21273/JASHS.138.3.159

    Article  Google Scholar 

  • Wielgoss A, Tscharntke T, Rumede A, Fiala B, Seidel H, Shahabuddin S, Clough Y (2014) Interaction complexity matters: disentangling services and disservices of ant communities driving yield in tropical agroecosystems. Proceed Royal Soc B: BiolSci 281:20132144

    Article  Google Scholar 

  • Young AM, Erickson EH, Strand MA et al (1987) Pollination biology of Theobroma and Herrania (Sterculiaceae)—I. Floral Biology. Int J Trop Insect Sci 8:151–164. https://doi.org/10.1017/s1742758400007153

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to the owners of the farms and home gardens that kindly allowed us to work on their lands. We also thank Pablo Isaías Cerda and Polibio Tapuy for helping us in the field and Karla Vera and Sofia Narváez for their help separating insects in the laboratory. We are very grateful to Eduardo Amat for the identification of the common insects and to Luciano Hildebrand for the English review of the manuscript and finally, to the German Technical cooperation GTZ for partially financing this research.

Funding

Funding was provided by Deutsche Gesellschaft für Internationale Zusammenarbeit.

Author information

Authors and Affiliations

  1. Faculty of Life Sciences, Universidad Regional Amazónica Ikiam, Tena, Ecuador

    Juan Ponce-Sánchez, María Gabriela Zurita-Benavides & María Cristina Peñuela

  2. Grupo de Ecosistemas Tropicales y Cambio Global, Km 8 vía a Muyuna, Tena, Napo, Ecuador

    María Gabriela Zurita-Benavides & María Cristina Peñuela

Authors
  1. Juan Ponce-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María Gabriela Zurita-Benavides
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María Cristina Peñuela
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JPS, MGZ and MCP contributed to the study conception and design; JPS prepared the material, collected field data, performed data analysis and wrote the initial (in Spanish) manuscript; MCP examined the structure and development of the study, managed to obtain financial support for the project and reviewed the manuscript several times; JPS and MGZ commented on previous versions of the manuscript; MCP coordinated and financed the experiment related to the pollinators; all authors read and approved the final manuscript.

Corresponding author

Correspondence to María Cristina Peñuela.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ponce-Sánchez, J., Zurita-Benavides, M.G. & Peñuela, M.C. Reproductive ecology of white cacao (Theobroma bicolor Humb. & Bonpl.) in Ecuador, western Amazonia: floral visitors and the impact of fungus and mistletoe on fruit production. Braz. J. Bot 44, 479–489 (2021). https://doi.org/10.1007/s40415-021-00709-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-021-00709-9

Keywords

Search

Navigation