SciELO - Scientific Electronic Library Online

 
 número129Una nueva especie de Miconia (Melastomataceae) de los bosques altoandinos de Bogotá D.C., ColombiaPrimer registro del hongo briófilo Paruephaedria heimerlii (Dactylosporaceae, Ascomycota) para México índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Acta botánica mexicana

versión On-line ISSN 2448-7589versión impresa ISSN 0187-7151

Act. Bot. Mex  no.129 Pátzcuaro  2022  Epub 30-Jun-2022

https://doi.org/10.21829/abm129.2022.2001 

Nota científica

Visit frequency of Euglossine bees (Hymenoptera: Apidae) to mature fruits of Vanilla planifolia (Orchidaceae)

Frecuencia de visita de Euglosinos (Hymenoptera: Apidae) a frutos maduros de Vanilla planifolia (Orchidaceae)

Miguel Ángel Lozano Rodríguez1 
http://orcid.org/0000-0003-0666-1822

Mauricio Luna Rodríguez1 
http://orcid.org/0000-0002-1204-9608

Juan Manuel Pech Canché2 
http://orcid.org/0000-0002-8455-593X

Rebeca Alicia Menchaca García3 
http://orcid.org/0000-0002-4241-8304

Carlos Roberto Cerdán Cabrera1  4 
http://orcid.org/0000-0002-0498-2617

1Universidad Veracruzana, Facultad de Ciencias Agrícolas, Circuito González Aguirre Beltrán s.n., Zona Universitaria, 91000 Xalapa, Veracruz, Mexico.

2Universidad Veracruzana, Facultad de Ciencias Biológicas y Agropecuarias región Poza Rica-Tuxpan, carretera Tuxpan-Tampico km 7.5 s.n., Col. Universitaria, 92860 Tuxpan, Veracruz, Mexico.

3Universidad Veracruzana, Centro de Investigaciones Tropicales, José María Morelos 44, Col. Centro, 91000 Xalapa, Veracruz, Mexico.


Abstract

Background and Aims:

Visitation and fragrance collection in fruits of the genus Vanilla by Euglossine bees (Eulaema spp.) have previously been documented. However, in Vanilla planifolia, the most commonly cultivated species, this behavior has not yet been recorded. Thus, the objective of this study was to identify Euglossine visitors of the mature fruits of V. planifolia and to identify the frequency of these visitations.

Methods:

We held 11 observations set within a month (from March 6 to April 6, 2021) in an experimental Vanilla planifolia plantation with mature fruits of vanilla in Veracruz, Mexico. Each observation lasted for ten hours (from 8:00 to 18:00), representing a total of 110 hours sampling effort. During our observations we collected individuals of Euglossine bees directly from the mature fruits of vanilla to identify them at species level. We also recorded the frequency of Euglossini visits to mature fruits of V. planifolia.

Key results:

We identified five species belonging to three Euglossini genera visiting mature fruits of V. planifolia: Euglossa hemichlora, E. variabilis, Eulaema cingulata, E. polychroma, and Exaerete frontalis. The genus Eulaema had 72% of visits to V. planifolia fruits. Visitation frequency was dominated by Eulaema polychroma with 54% of total recorded visits (n=211).

Conclusions:

For the first time, Euglossine bees have been registered collecting scents in mature fruits of V. planifolia. Eulaema polychroma was the species with the highest percentage of visits to mature fruits V. planifolia to collect fragrances.

Key words: Euglossa; Eulaema; Exaerete; scent; vanilla

Resumen

Antecedentes y Objetivos:

Se ha reportado la visita y recolección de fragancias en frutos del género Vanilla por abejas Euglosinas (Eulaema spp.). Sin embargo, en Vanilla planifolia aun no se ha registrado este comportamiento. Por lo tanto, los objetivos del presente trabajo fueron identificar a los euglosinos que visitaban los frutos maduros de V. planifolia, así como la frecuencia de su visita.

Métodos:

Se llevaron a cabo 11 muestreos durante un mes (6 de marzo al 6 de abril de 2021) en una plantación experimental de Vanilla planifolia con frutos maduros de vainilla en Veracruz, México. Cada muestreo tuvo una duración de diez horas (08:00 a 18:00 hrs), representando en total 110 horas de esfuerzo de muestreo. Durante los muestreos se colectaron individuos de abejas Euglosinas directamente de los frutos maduros de vainilla para identificarlos a nivel de especie. También se registró la frecuencia de visita por parte de los euglosinos a los frutos maduros de V. planifolia.

Resultados clave:

Se identificaron cinco especies pertenecientes a tres géneros de Euglossini que visitaban los frutos maduros de Vanilla planifolia: Euglossa hemichlora, E. variabilis, Eulaema cingulata, E. polychroma y Exaerete frontalis. El género Eulaema representó 72% de las visitas a los frutos de V. planifolia. A su vez, la frecuencia de visita estuvo dominada por Eulaema polychroma con 54% del total de las vistas registradas (n=211).

Conclusiones:

Por primera vez se registran abejas Euglosinas colectando fragancias de los frutos maduros de V. planifolia. Eulaema polychroma es la especie con el mayor porcentaje de visita a los frutos maduros de V. planifolia para recolectar fragancias.

Palabras clave: Euglossa; Eulaema; Exaerete; fragancias; vainilla

Introduction

Orchid bees depend strongly on resources like resins and scents for the construction of nests and attracting mates, respectively (Roubik and Hanson, 2004). It is also known that orchid bees collect scents from non-floral sources, like sap from plant wounds, fruits, and cadavers of other male Euglossine bees (Roubik and Hanson, 2004), as well as from fungi (Cappellari and Harter-Marques, 2010). Scent collection is exclusively performed by male Euglossine bees (Dodson et al., 1969; Roubik and Hanson, 2004). This process consists of scraping the structure surface with their front tarsi followed by fluttering, while the chemical transfers from the front tarsus to the middle tarsi and then to the posterior tibia. Afterwards, the bees land on the source of the scent scraping the surface, repeating this behavior for up to one hour (Roubik and Hanson, 2004). This process of scent collection by male Euglossine bees has been studied for at least five decades (e.g., van der Pijl and Dodson, 1966; Dressler, 1967). More recent studies have focused on the interactions between Euglossine bees and orchid flowers and their fragrances (e.g., Ramírez et al., 2002; Roubik and Hanson, 2004; Hentrich, 2008; Hetherington-Rauth and Ramírez, 2016; Nunes et al., 2017; Milet-Pinheiro et al., 2018; Pansarin et al., 2018).

Chemical baits are being used to attract and identify Euglossine bees. One of the main attractors used is eucalyptol (Dodson et al., 1969; Dressler, 1982; Silva and Rebêlo, 2002; Ferreira et al., 2011; Silva, 2012; Castro et al., 2013; Ribeiro et al., 2015), and vanillin has also been used in chemical baits for euglossines (Williams and Dodson, 1972; Dressler, 1982; Dressler, 1993; Rebêlo and Silva, 1999; Ramírez et al., 2002; Silva and Rebêlo, 2002; Melo et al., 2009; Ferreira et al., 2011; Silva, 2012; Castro et al., 2013; Hinojosa-Díaz and Engel, 2014; Pansarin et al., 2018; Coswosk et al., 2019; Dec and Alves-Dos-Santos, 2019). However, relatively few orchid species naturally produce flowers with vanillin scent (Williams and Dodson, 1972; Gerlach and Schill, 1991). This scent is produced by vanilla fruits, rather than by flowers.

Lubinsky et al. (2006 reported Eulaema cingulata Fabricius, 1804 collecting scents from fruits of Vanilla grandiflora Lindl. (=V. pompona subsp. grandiflora (Lindl.) Soto Arenas) and E. cingulata has been recorded being attracted to vanillin in chemical baits (e.g., Ramírez et al., 2002; Silva and Rebêlo, 2002; Melo et al., 2009; Silva, 2012; Coswosk et al., 2019; Dec and Alves-Dos-Santos, 2019). However, this has not yet been observed in Vanilla planifolia Andrews. Considering that mature fruits of V. planifolia naturally produce vanillin, we hypothesized that E. cingulata will be the species with the highest visiting frequency to collect scents from the mature fruits of V. planifolia. Therefore, the objective was to identify Euglossine species and visitation frequency to mature fruits of V. planifolia.

Materials and Methods

The study was carried out in an experimental Vanilla planifolia plantation established in 2013, which has trees of Inga vera Willd. and shrubs of Coffea arabica L. as live tutors. This plantation is located in Jilotepec, Veracruz, Mexico, at 1000 m above sea level (Fig. 1). Eleven observations were done within a month (March 6 to April 6, 2021) every fourth day. Mature fruits were approximately 12 months old (2020 bloom). Each observation lasted ten hours (8:00 to 18:00), representing a total of 110 hours sampling effort. During our observations we collected individuals of Euglossine bees directly from V. planifolia mature fruits to identify them at species level. Species identification and sex determination were done for each of the collected specimens. Euglossine bees were identified using the taxonomic keys of Roubik and Hanson (2004) and Estrada de L. (2018). We also registered Euglossine bee visit frequency to mature V. planifolia fruits and their behavior through the observations. These visits were recorded with photographs and video using a Nikon D3100 digital SLR camera (Nikon, Tokyo, Japan). Visit frequency data were analyzed using a (2 in R v. 4.0.3 (R Core Team, 2020).

Figure 1: Map of the experimental Vanilla planifolia Andrews plantation in Jilotepec, Veracruz de Ignacio de la Llave, Mexico.  

Results

We collected five species (15 individuals) visiting the mature fruits of V. planifolia to collect scents. They belonged to three genera of Euglossine bees (Euglossa Latreille, 1802; Eulaema Lepeletier, 1841; and Exaerete Hoffmannsegg, 1817) (Fig. 2). The five species were Euglossa hemichlora Cockerell, 1917; E. variabilis Friese, 1899; Eulaema cingulata, E. polychroma Mocsáry, 1899 and Exaerete frontalis Guérin-Meneville, 1845 (Fig. 3). All of them were male specimens.

Figure 2: Attraction and collection of scents in mature fruits Vanilla planifolia Andrews. A. Euglossa Latreille, 1802; B. Eulaema Lepeletier, 1841; C. Exaerete Hoffmannsegg, 1817. Photos: M. A. Lozano Rodríguez. 

Figure 3: Euglossine species attracted to mature fruits of Vanilla planifolia Andrews. A. Euglossa hemichlora Cockerell, 1917; B. Euglossa variabilis Friese, 1899; C. Eulaema cingulata Fabricius, 1804; D. Eulaema polychroma Mocsáry, 1899; E. Exaerete frontalis Guérin-Meneville, 1845. Photos: M. A. Lozano Rodríguez. 

The genus Eulaema reported 72% of the visits to V. planifolia mature fruits (n=211), while Euglossa and Exaerete had 27% and 1% of these, respectively. Eulaema polychroma was the species with the highest visitation frequency (54% of total visits), followed by Eulaema cingulata with 18%. The visitation frequency for Euglossa was not calculated at the species level because of the difficulty to visually distinguish them in this genus without collecting and analyzing each specimen. We were thus only able to identify two species from five individuals that we collected. We found statistically significant differences (Table 1) in the visitation frequency of Euglossine bees (X 2=20.65; gl=2; p<0.001). Exaerete frontalis was not included in the statistical analysis because of its low visitation frequency (1%, n=2).

Table 1: Total visits by Euglossine bees to mature fruits of Vanilla planifolia Andrews recorded during this study on a vanilla plantation in Jilotepec, Veracruz, Mexico. *Not included in the statistical analysis. 

Genus Species Visits Total visits by genus
Euglossa Latreille, 1802 Euglossa spp. 58 58
Eulaema Lepeletier, 1841 Eulaema cingulata Fabricius, 1804 38 151
Eulaema polychroma Mocsáry, 1899 113
Exaerete Hoffmannsegg, 1817 Exaerete frontalis Guérin-Meneville, 1845* 2 2

Discussion

The individuals of the three genera observed in the mature fruits of V. planifolia performed the typical scent collection behavior described by Roubik and Hanson (2004). This behavior has been recorded for mature fruits of Vanilla pompona subsp. grandiflora (Lubinsky et al., 2006) and V. aff. odorata (Madison, 1981) but, to our knowledge, the present study reported it for the first time for V. planifolia.

According to various studies (Williams and Dodson, 1972; Dressler, 1982; Rebêlo and Silva, 1999; Ramírez et al., 2002; Silva and Rebêlo, 2002; Melo et al., 2009; Silva, 2012; Castro et al., 2013; Hinojosa-Díaz and Engel, 2014; Coswosk et al., 2019; Dec and Alves-Dos-Santos, 2019), the use of vanillin as an attractor has been effective in approximately 179 Euglossine species. Four of these (Euglossa variabilis, Eulaema cingulata, E. polychroma, and Exaerete frontalis) have been observed naturally in our study in mature fruits of V. planifolia. Euglossa hemichlora is the only one that has not been previously reported as attracted to vanillin. Even when E. cingulata is the species that has been more times recorded being attracted to vanillin using chemical baits (Ramírez et al., 2002; Silva and Rebêlo, 2002; Melo et al., 2009; Silva, 2012; Coswosk et al., 2019; Dec and Alves-Dos-Santos, 2019), our field observations found E. polychroma as the bee with the greatest visiting frequency collecting scents from the mature fruits of V. planifolia. Consequently, with these results we reject our hypothesis, as E. cingulata was not the species with the greatest records. Even when both species can be found in Veracruz (Mexico) (Yáñez-Ordóñez and Hinojosa-Díaz, 2004; Bonet and Vergara, 2019; Juárez, 2021), our study shows that E. polychroma is the one who is more attracted to mature fruits of V. planifolia.

Euglossine bees have been reported collecting scents in fruits and pollinating Vanilla flowers (Soto, 1999; Lubinsky et al., 2006; Watteyn et al., 2021), and this study shows that V. planifolia fruits attract orchid bees to collect scents as well. Therefore, it might be the only genus in the Orchidaceae family that has this double interaction with orchid bees. In general, these bees’ visitation frequency to the fragrant fruit of vanilla had not been previously studied in detail. Moreover, the potential role of orchid bees as disperser of the seeds of Vanilla species with aromatic fruits has been suggested (Madison, 1981; Dressler, 1993; Lubinsky et al., 2006; van Dam et al., 2010; Cameron, 2011).

Exaerete frontalis was the rarest species with the lowest visiting frequency to mature fruits of V. planifolia. Similarly, Rebêlo and Silva (1999) and Ramírez et al. (2002) found that Exaerete frontalis is rarely attracted to vanillin. Parasitic genera (like Exaerete) have seldomly been documented to be interacting with orchids (Roubik and Hanson, 2004). However, in this study we were able to observe this unusual interaction between E. frontalis and the mature fruits of V. planifolia to collect scents.

Conclusions

For the first time orchid bees have been registered collecting scents in mature fruits of V. planifolia. The genus Eulaema is strongly attracted to the mature fruits of V. planifolia to collect scents. Eulaema polychroma was the species with greatest attraction and interaction with the mature fruits of V. planifolia, even when E. cingulata was the species with more records of being attracted to vanillin and mature fruits of vanilla. All the species performed the typical behavior of scent collection by orchid bees. The visiting dynamics of Euglossine bees requires further studies to understand their behavior during the process of attraction-visit-collection of scent of the fruit of V. planifolia.

Acknowledgements

We thank Gerardo Quintos for the identification of Euglossine species. Also, we appreciate the help of Raíces de la Montaña for the map. We are very grateful to the reviewers and the editorial committee who contributed to improve the manuscript. MALR thanks Doctorado en Ciencias Agropecuarias, and CONACyT for the PhD scholarship (CVU: 399340).

Literature cited

Bonet, F. M. and C. H. Vergara. 2019. Abejas silvestres de un cafetal orgánico en Veracruz, México. Universidad de las Américas Puebla. Puebla, México. 517 pp. [ Links ]

Cameron, K. M. 2011. Vanilla orchids. Natural History and Cultivation. Timber Press. Oregon, USA. 212 pp. [ Links ]

Cappellari, S. C. and B. Harter-Marques. 2010. First report of scent collection by male orchid bees (Hymenoptera: Apidae: Euglossini) from terrestrial mushrooms. Journal of the Kansas Entomological Society 83(3): 264-266. DOI: https://doi.org/10.2317/JKES0911.16.1 [ Links ]

Castro, M. M. do N., C. A. Garófalo, J. C. Serrano and C. I. Silva. 2013. Temporal variation in the abundance of Orchid Bees (Hymenoptera: Apidae) in a Neotropical Hygrophilous Forest. Sociobiology 60(4): 405-412. [ Links ]

Coswosk, J. A., E. D. G. Soares and L. R. R. Faria. 2019. Bait traps remain attractive to euglossine bees even after two weeks: a report from Brazilian Atlantic forest. Revista Brasileira de Entomologia 63(1): 1-5. DOI: https://doi.org/10.1016/j.rbe.2018.11.001 [ Links ]

Dec, E. and I. Alves-Dos-Santos. 2019. Species distribution of Euglossini bees (Hymenoptera: Apidae) at an altitudinal gradient in Northern Santa Catarina. Sociobiology 66(4): 568-574. DOI: https://doi.org/10.13102/sociobiology.v66i4.3436 [ Links ]

Dodson, C. H., R. L. Dressler, H. G. Hills, R. M. Adams and N. H. Williams. 1969. Biologically active compounds in orchid fragrances. Science 164(3885): 1243-1249. DOI: https://doi.org/10.1126/science.164.3885.1243 [ Links ]

Dressler, R. L. 1967. Why do euglossine bees visit orchid flowers? Atas Do Simpósio Sôbre a Biota Amazônica 5: 171-180. [ Links ]

Dressler, R. L. 1982. Biology of the orchid bees (Euglossini). Annual Review of Ecology and Systematics 13: 373-394. DOI: https://doi.org/10.1146/annurev.es.13.110182.002105 [ Links ]

Dressler, R. L. 1993. Phylogeny and Classification of the Orchid Family. Dioscorides Press. Oregon, USA. 314 pp. [ Links ]

Estrada de L., C. M. 2018. Las abejas del género Euglossa (Hymenoptera: Apidae: Euglossini) de México. Tesis de maestría. Facultad de Ciencias, Universidad Autónoma de México. Cd. Mx., México. 96 pp. [ Links ]

Ferreira, M. G., O. C. de Pinho, J. B. P. Balestieri and O. Faccenda. 2011. Fauna and stratification of male orchid bees (Hymenoptera: Apidae) and their preference for odor baits in a forest fragment. Neotropical Entomology 40(6): 639-646. [ Links ]

Gerlach, G. and R. Schill. 1991. Composition of Orchid Scents Attracting Euglossine Bees. Plant Biology 104(5): 379-384. DOI: https://doi.org/10.1111/j.1438-8677.1991.tb00245.x [ Links ]

Hentrich, H. 2008. The reproductive biology of euglossine-pollinated plants in the Natural Reserve Nouragues, French Guiana. Doktorarbeit. Fakultät für Naturwissenschaften der Universität Ulm. Ulm, Deutschland. 177 pp. DOI: http://doi.org/10.18725/OPARU-1163 [ Links ]

Hetherington-Rauth, M. C. and S. R. Ramírez. 2016. Evolution and diversity of floral scent chemistry in the euglossine bee-pollinated orchid genus Gongora. Annals of Botany 118(1): 135-148. DOI: https://doi.org/10.1093/aob/mcw072 [ Links ]

Hinojosa-Díaz, I. A. and M. S. Engel. 2014. Revision of the orchid bee subgenus Euglossella (Hymenoptera: Apidae), part II: The viridis and mandibularis species groups. Journal of Melittology 36: 1-108. DOI: https://doi.org/10.17161/jom.v0i36.4777 [ Links ]

Juárez R., D. A. 2021. Revisión de la tribu Euglossini (Hymenoptera: Apidae) en México, con énfasis en la fauna de la Estación de Biología tropical de Los Tuxtlas, Veracruz, México. Tesis de licenciatura. Facultad de Ciencias, Universidad Nacional Autónoma de México. Cd. Mx., México. 314 pp. [ Links ]

Lubinsky, P., M. Van Dam and A. Van Dam. 2006. Pollination of Vanilla and evolution in Orchidaceae. Lindleyana 75(12): 926-929. [ Links ]

Madison, M. 1981. Vanilla beans and bees. Bulletin Marie Selby Botanical Gardens 8: 8. [ Links ]

Melo, P. N., M. Gimenes and A. O. Neto. 2009. Daily activity patterns of visits by males of four species of Eulaema (Apidae: Euglossina) to odor baits in a tropical forest fragment in Bahia, Brasil. Zoologia 26(2): 204-212. DOI: https://doi.org/10.1590/S1984-46702009000200002 [ Links ]

Milet-Pinheiro, P., J. B. F. Silva, D. M. A. F. Navarro, I. C. S. Machado and G. Gerlach. 2018. Notes on pollination ecology and floral scent chemistry of the rare neotropical orchid Catasetum galeritum Rchb. f. Plant Species Biology 33(2): 158-163. DOI: https://doi.org/10.1111/1442-1984.12202 [ Links ]

Nunes, C. E. P., M. Wolowski, E. R. Pansarin, G. Gerlach, I. Aximoff, N. J. Vereecken, M. J. Salvador and M. Sazima. 2017. More than euglossines: the diverse pollinators and floral scents of Zygopetalinae orchids. Die Naturwissenschaften 104: 92. DOI: https://doi.org/10.1007/s00114-017-1511-3 [ Links ]

Pansarin, L. M., E. R. Pansarin , G. Gerlach and M. Sazima. 2018. The natural history of Cirrhaea and the pollination system of Stanhopeinae (Orchidaceae). International Journal of Plant Sciences 179(6): 436-449. DOI: https://doi.org/10.1086/697997 [ Links ]

R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Viena, Austria. https://www.R-project.org/ (consultado julio de 2021). [ Links ]

Ramírez, S., R. L. Dressler and M. Ospina. 2002. Abejas euglosinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notas sobre su biología. Biota Colombiana 3(1): 1-118. [ Links ]

Rebêlo, J. M. M. and F. S. Silva. 1999. Distribuição das abelhas Euglossini (Hymenoptera: Apidae) no estado do Maranhão, Brasil. Anais Da Sociedade Entomológica Do Brasil 28(3): 389-401. DOI: https://doi.org/10.1590/s0301-80591999000300003 [ Links ]

Ribeiro F., L. R., N. V. Sydney and R. Barbosa. 2015. How Brazilian researchers have been sampling orchid bees? In: Aguiar, A. J. C., R. B. Gonçalves and K. S. Ramos (Orgs.) Ensaios sobre as Abelhas da Região Neotropical. Curitiba, Brasil. Pp. 307-346. [ Links ]

Roubik, D. W. and P. E. Hanson. 2004. Orchid bees of tropical America. Biology and field guide. Editorial INBio. Santo Domingo de Heredia, Costa Rica. 352 pp. [ Links ]

Silva, F. S. 2012. Orchid bee (Hymenoptera: Apidae) community from a gallery forest in the Brazilian Cerrado. Revista de Biologia Tropical 60(2): 625-633. DOI: https://doi.org/10.15517/rbt.v60i2.3949 [ Links ]

Silva, F. S. and J. M. M. Rebêlo. 2002. Population dynamics of Euglossinae bees (Hymenoptera, Apidae) in an early second-growth forest of Cajual Island, in the state of Maranhão, Brazil. Brazilian Journal of Biology 62(1): 15-23. DOI: https://doi.org/10.1590/S1519-69842002000100003 [ Links ]

Soto A., M. A. 1999. Filogeografía y recursos genéticos de las vanillas de México. Instituto Chinoin, A.C. Cd. Mx., México. 106 pp. [ Links ]

van Dam, A. R., J. E. Householder and P. Lubinsky. 2010. Vanilla bicolor Lindl. (Orchidaceae) from the Peruvian Amazon: Auto-fertilization in Vanilla and notes on floral phenology. Genetic Resources and Crop Evolution 57(4): 473-480. DOI: https://doi.org/10.1007/s10722-010-9540-1 [ Links ]

van der Pijl, L. and C. H. Dodson. 1966. Orchid flowers: their pollination and evolution. University of Miami Press. Coral Gables, USA. 213 pp. [ Links ]

Watteyn, C., D. Scaccabarozii, B. Muys, N. Van der Schueren, K. Van Meerbeek, M. F. Guizar Amador, J. D. Ackerman, M. Cedeño Fonseca, I. Chinchilla Alvarado, B. Reubens, R. Pillco Huarcaya, S. Conzzolino and A. Karremans. 2021. Trick or Treat? Pollinator attraction in Vanilla pompona (Orchidaceae). Biotropica 54: 268-274. DOI: https://doi.org/10.1111/btp.13034 [ Links ]

Williams, O. H. and C. H. Dodson . 1972. Selective attraction of euglossine bees to orchid floral fragrances and its importance in long distance pollen flow. Evolution 26: 84-95. DOI: https://doi.org/10.2307/2406985 [ Links ]

Yáñez-Ordóñez, S. and I. Hinojosa-Díaz. 2004. La colección himenopterológica (Insecta) del Museo de Zoología "Alfonso L. Herrera" de la Facultad de Ciencias, UNAM, México. Acta Zoológica Mexicana 20: 167-197. [ Links ]

Author contributions

MALR, CCC and MLR conceived the study design and carried out the field work. JPC carried out the data analysis. MALR, CCC and MLR wrote the manuscript. MLR, CCC, JPC and RMG revised and completed the manuscript. All authors contributed to the discussion and approval of the final manuscript.

Funding

This study was supported by scholarship number 791316 of the 2021-1 program of the Padrón Nacional de Posgrados de Calidad, of the Consejo Nacional de Ciencia y Tecnología (CONACyT) granted to MALR.

Received: November 29, 2021; Revised: January 13, 2022; Accepted: April 05, 2022; Published: April 08, 2022

4Author for correspondence: ccerdan@uv.mx

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License