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Bee–Plant Interactions: Competition and Phenology of Flowers Visited by Bees

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Biodiversity and Conservation of the Yucatán Peninsula

Abstract

We present results of the flowering phenology of most plant species visited by European and Africanized honey bee (Apis mellifera ligustica and A. mellifera scutellata, respectively) in the Yucatán Peninsula. Colonies from both bee types visited the largest number of plant species at the end of the wet season (September and October) and the beginning of the dry season (November). A calendar is presented to indicate the community phenology of the floral resources of Apis mellifera. Comparisons were made in order to assess potential competition between both honey bee groups and between honey bees and native bees in relation to their food resources. Trees were also a constant pollen resource for Apis mellifera and Melipona beecheii, a native stingless bee. Solitary bees and M. beecheii bee seemed to change their floral resource use, both show ‘resource partitioning’ to avoid competition. For example, two important plant families, Anacardiaceae and Euphorbiaceae, were lost to competing honey bees, but compensated for by greater use of Fabaceae, Rubiaceae, and Sapotaceae among solitary bees. Invasive generalist pollinators may, however, cause specialized competitors to fail, especially in less biodiverse environments. Deforestation, hurricanes, and fires are three factors that affect the habitat and food resources for bee colonies. Within agricultural areas, having large areas of natural vegetation, corridors, or strips of vegetation between the crop fields is important to favor adequate diversity of natural pollinators for pollination of crop plants.

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References

  • Ashworth L, Quesada M, Casas A, Aguilar R, Oyama K. Pollinator-dependent food production in Mexico. Biol Conserv. 2009;142:1050–7.

    Article  Google Scholar 

  • Barrios-Delgado C, Pérez-Dominguez E, Sánchez-Navarro LM. Efectos y repercusiones de la abeja africana en la Península de Yucatán. In: Proceedings of the IV American Seminar on beekeeping, Mazatlán, Sinaloa. Secretaría de Agricultura y Recursos Hidráulicos and Gobierno del estado de Sinaloa, Mexico; 1990, p. 15–33.

    Google Scholar 

  • Borchert R, Meyer SA, Felger RS, Porter-Bolland L. Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Glob Ecol Biogeogr. 2004;13:409–25.

    Article  Google Scholar 

  • Burkle LA, Alarcón R. The future of plant—pollinator diversity: understanding interaction networks across time, space, and global change. Am J Bot. 2011;98(3):1–11.

    Article  Google Scholar 

  • Cairns CE, Villanueva-Gutiérrez R, Koptur S, Bray DB. Bee populations, forest disturbance, and Africanization in Mexico. Biotropica. 2005;37(4):686–92.

    Article  Google Scholar 

  • Calkins CF. The introduction of A. mellifera to the Yucatán Peninsula of Mexico. Gleanings in Bee Culture. 1975;103:202–3.

    Google Scholar 

  • Ceballos-Martínez VM. Evaluación del polen recolectado por la abeja Apis mellifera ligustica Spinola en la Resrva de la Biósfera de Sian Ka'an, Quintana Roo, México. Bch thesis. University of Veracruz; Córdoba, Ver., Mexico; 1987, p. 24.

    Google Scholar 

  • Daly HV, Balling SS. Identification of Africanized honeybees in the Western Hemisphere by discriminant analysis. J Kansas Entomol Soc. 1978;5:857–69.

    Google Scholar 

  • Echazarreta CM, Quezada-Euan JJG, Medina LM, Pasteur KL. Beekeeping in the Yucatán Peninsula: development and current status. Bee World. 1997;78(3):115–27.

    Article  Google Scholar 

  • Erdtman G. An introduction to pollen analysis. Waltham, MA: Chronica Botánica Co.;1943. 239p.

    Google Scholar 

  • Galindo-Cardona A, Acevedo-Gonzalez JP, Rivera-Marchard B, Giray T. Genetic structure of the gentle Africanized honey bee population (gAHB) in Puerto Rico. BMC Genet. 2013;14:65.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gentry AH. Diversity and floristic composition of neotropical dry forests. In: Bullock SH, Mooney HA, Medina F, editors. Seasonally dry tropical forests. Cambridge: Cambridge University Press; 1995.

    Google Scholar 

  • Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T. Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci. 2007;274(1608):303–13.

    Article  Google Scholar 

  • Koeppen W. Das gepographische system der klimate in handbuch der klimatologie. Band I, Teil C; Berlin, Germany; 1936. p. 44.

    Google Scholar 

  • Kuswaha CP, Tripathi SK, Tripathi BD, Singh KP. Patterns of tree phenological diversity in dry tropics. Acta Ecol Sin. 2013;31:179–85.

    Article  Google Scholar 

  • Labougle-Rentería JM, Zozaya- Rubio JA. La apicultura en México. Ciencia y Desarrollo. 1986;69:17–35.

    Google Scholar 

  • Levin MD, Glowska-Konopacka S. Responses of foraging honeybees in alfalfa to increasing competition from other colonies. J Apic Res. 1963;2(1):33–42.

    Google Scholar 

  • Lieth H. Phenology and seasonality modeling. Ecological studies, vol. 8. New York: Springer; 1974.

    Book  Google Scholar 

  • Meléndez-Ramírez V, Magaña-Rueda S, Parra-Tabla V, Ayala R, Navarro J. Diversity of native bee visitors of cucurbit crops (Cucurbitaceae) in Yucatán México. J Insect Conserv. 2002;6(135–147):2002.

    Google Scholar 

  • Miranda F, Hernández-X J. Los tipos de vegetación de México y su clasificación. Bol Soc Bot Méx. 1963;28:29–179.

    Google Scholar 

  • Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals? Oikos. 2011;120(3):321–6.

    Article  Google Scholar 

  • O'Rourke MK, Buchmann SL. Standardized analytical techniques for bee-collected pollen. Entomol Soc Am. 1991;20:507–13.

    Google Scholar 

  • Palacios Chávez R, Ludlow-Wiechers B, Villanueva-Gutiérrez R. Flora palinológica de la Reserva de la Biosfera de Sian Ka'an, Quintana Roo, México. Mexico: Centro de Investigaciones de Quintana Roo;1991. 321 pp.

    Google Scholar 

  • Parra-Romero HI. Recursos poliníferos de importancia para la abeja Melipona beecheii durante el período húmedoen el campus de ECOSUR, Chetumal. Bch. thesis. Instituto Tecnológico de Chetumal. Chetumal, Quintana Roo, Mexico; 2015.

    Google Scholar 

  • Parra-Tabla V, Vargas CF. Phenology and phenotypic natural selection on the flowering time of a deceit-pollinated tropical orchid, Myrmecophila christinae. Ann Bot. 2004;94:243–50.

    Article  PubMed Central  PubMed  Google Scholar 

  • Paxton RJ, Echazarreta-González C, García M. Africanized honey bees in Yucatán, Mexico: a detailed survey. Am Bee J. 1991;131:646–8.

    Google Scholar 

  • Porter-Bolland L. La apicultura y el paisaje maya. Estudio sobre la fenología de floración de las especies melíferas y su relación con el ciclo apícola en La Montaña, Campeche, México. JSTOR. University of California Press, Mexican Studies-Estudios mexicanos. 2003;19(2):303–30.

    Article  Google Scholar 

  • Porter-Bolland L. Estudio de caso: flora melífera de Campeche. En: Villalobos-Zapata, GJ, Mendoza Vega J. (Coord.), 2010. La Biodiversidad de Campeche: Estudio de Estado. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO), Gobierno del Estado de Campeche, Universidad Auónoma de Campeche, El Colegio de la Frontera Sur. Mexico. Pg; 2010.

    Google Scholar 

  • Porter-Bolland L, Medina Abreo ME, Montoy-Koh P, Martín-Ek G, May Pacheco G. Flora Melífera de la Montaña, Campeche: su importancia para la apicultura y la vida diaria. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad e Instituto de Ecología, A. C., Xalapa, Ver. México; 2009, p. 322 ISBN: 978-607-7579-11-3.

    Google Scholar 

  • Rico-Gray V, Chemas A, Mardujano S. Uses of tropical deciduous forest species by the Yucatecan Maya. Agr Syst. 1991;14:149–61.

    Article  Google Scholar 

  • Roubik DW. Ecology and natural history of tropical bees. Cambridge: Cambridge University Press; 1989.

    Book  Google Scholar 

  • Roubik DW. Pollination of cultivated plants in the tropics. Agricultural Services Bulletin 1118. Rome: FAO; 1995.

    Google Scholar 

  • Roubik DW. Ecological impact on native bees by the invasive Africanized honey bee. Acta Biol Colombiana. 2009;14(2):114–24.

    Google Scholar 

  • Roubik DW, Villanueva-Gutiérrez R. Invasive Africanized honey bee impact on native solitary bees: a pollen resource and trap nest analysis. Biol J Linn Soc. 2009;98:152–60.

    Article  Google Scholar 

  • Roubik D W, Sakai S, Hamid AA, editors. Pollination ecology and the rain forest. Ecological studies 174. Sarawak Studies. New York: Springer; 2005.

    Google Scholar 

  • Roubik DW, editor. Pollinator safety in agriculture. Rome: FAO and UNEP; 2014.

    Google Scholar 

  • Roubik DW, Bernhardt P, Meier S. Orchids and Neotropical tropical pollinators, since Darwin’s time. In: Darwin’s orchids: then and now. Chicago: University of Chicago Press; 2014. p. 229–61.

    Google Scholar 

  • Salinas-Peba L, Parra-Tabla V. Phenology and pollination of Manilkara zapota in forest and homegardens. Forest Ecol Manage. 2007;248:136–42.

    Article  Google Scholar 

  • Smith MV, Adie A. A new design in pollen traps. Can Bee J. 1963; 74: 4,5,8.

    Google Scholar 

  • Vergara C. Rango de vuelo y cuantificación de los recursos colectados por abejas africanizadas en un bosque tropical de Panamá. Unpublished data report. Balboa, Panama: Smithsonian Tropical Research Institute; 1983.

    Google Scholar 

  • Villanueva-Gutiérrez R. Plantas de importancia apícola en el ejido de Plan del Río, Veracruz, México. Biotica. 1984;9(3):279–340.

    Google Scholar 

  • Villanueva-Gutiérrez R. Nectar sources of European and Africanized honeybees (Apis mellifera L.) in the Yucatán Peninsula, Mexico. J Apic Res. 1994;33(1):44–58.

    Google Scholar 

  • Villanueva-Gutiérrez R. Pollen resources used by European and Africanized honey bees in the Yucatán Peninsula, Mexico. J Apic Res. 1999;38(1–2):105–11.

    Google Scholar 

  • Villanueva-Gutiérrez R. Polliniferous plants and foraging strategies of Apis mellifera in the Yucatán Peninsula, Mexico. Rev Biol Trop. 2002;50(3/4):1035–44.

    Google Scholar 

  • Villanueva-Gutiérrez R, Roubik DW. Why are African honey bees and not European bees invasive? Pollen diet diversity in community experiments. Apidologie. 2004;35:481–91.

    Article  Google Scholar 

  • Villanueva-Gutiérrez R, Colli Ucán W. Plantas nectaríferas visitadas por la abeja maya Xunancab (Melipona beecheii) en Quintana Roo. Proceedings of the XIX American Seminario of Beekeeping, Campeche, Campeche. SAGARPA, Unión Nacional de Apicultores and Gobierno del Estado de Campeche; 2005.

    Google Scholar 

  • Villanueva-Gutiérrez R, Buchamann S, Donovan AJ, Roubik DW. Crianza y manejo de la abeja xunancab en la Península de Yucatán. Tucson Arizona: ECOSUR-The BEE Works; 2005a.

    Google Scholar 

  • Villanueva-Gutiérrez R, Roubik WD, Colli-Ucán W. Extinction of Melipona beecheii and traditional beekeeping in the Yucatán Peninsula. Bee World. 2005b;86(2):35–41

    Google Scholar 

  • Villanueva-Gutiérrez R, Echazarreta González C, Roubik DW, Moguel-Ordoñez Y. Transgenic soybean pollen (Glycine max L.) in honey from the Yucatán Peninsula, Mexico. Scientific Rep. 2014; 4: 4002.

    Google Scholar 

  • Visscher PK, Seeley TD. Foraging strategy of honey bee colonies in a temperate deciduous forest. Ecology. 1982;63:1790–801.

    Article  Google Scholar 

  • Waller GD. A modification of the O.A.C. pollen trap. Am Bee J. 1980;120:119–21.

    Google Scholar 

  • Winston M. The biology of the honey bee. Cambridge, MA: Harvard University Press;1987. 281p.

    Google Scholar 

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Correspondence to Rogel Villanueva-Gutiérrez .

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Appendix

Appendix

1.1 Calendar of Plants Visited for Honey and Pollen Collection by Honey Bees (Sampling Period of 2 Years)

Angiospermae

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Acanthaceae

Bravaisia tubiflora

          

+

 

Justicia campechiana

+

 

+

  

+

+

+

+

+

+

+

Amaranthaceae

Amaranthus sp. 1

+

           

Iresine celosia

    

+

       

Anacardiaceae

Metopium brownei

+

+

+

+

+

+

+

 

+

+

+

+

Spondias sp. 1

     

+

+

     

Annonaceae

Annona sp. 1

         

+

  

Apocynaceae

Mandevilla sp. 1

    

+

       

Araliaceae

Dendropanax arboreus

        

+

+

+

 

Arecaceae

Chamaedorea sp. 1

       

+

+

 

+

 

Cocos nucifera

+

+

      

+

+

+

+

Thrinax radiata

   

+

        

Arecaceae 1

 

+

+

    

+

+

   

Arecaceae 2

 

+

     

+

    

Asteraceae

Baccharis heterophylla

+

           

Bidens squarrosa

+

+

    

+

     

Bidens sp. 1

+

      

+

+

+

+

+

Eupatorium albicaule

+

+

+

     

+

+

+

+

Eupatorium campechense

+

           

Eupatorium sp. 1

       

+

+

+

+

 

Eupatorium sp. 2

+

+

+

+

 

+

+

+

+

+

+

 

Melanthera aspera

 

+

 

+

+

+

 

+

+

+

+

+

Melanthera nivea

       

+

+

 

+

 

Mikania sp. 1

  

+

         

Parthenium hysterophorus

+

+

+

+

+

+

+

 

+

+

+

+

Pluchea sp. 1

+

 

+

+

  

+

+

+

+

+

+

Vernonia cinerea

+

+

          

Viguiera dentata

+

+

+

+

      

+

 

Asteraceae 1

+

           

Asteraceae 3

   

+

        

Asteraceae 4

  

+

         

Asteraceae 5

         

+

  

Bignoniaceae

Amphilophium paniculatum

 

+

    

+

 

+

+

+

 

Arrabidaea floribunda

        

+

 

+

 

Cydista sp. 1

       

+

  

+

 

Cydista sp. 2

       

+

+

   

Bignoniaceae 1

         

+

+

 

Bombacaceae

Ceiba aesculifolia

        

+

+

+

 

Ceiba pentandra

    

+

       

Pseudobombax ellipticum

+

 

+

+

+

 

+

  

+

+

+

Boraginaceae

Cordia alliodora

     

+

      

Cordia curassavica

       

+

+

   

Cordia dodecandra

+

          

+

Cordia gerascanthus

          

+

 

Cordia sp. 1

      

+

   

+

 

Cordia sp. 3

    

+

  

+

+

   

Cordia sp. 4

+

+

+

+

 

+

 

+

+

+

+

 

Cordia sp. 5

          

+

 

Heliotropium sp. 1

 

+

 

+

        

Heliotropium sp. 2

          

+

 

Burseraceae

Bursera simaruba

+

+

+

+

+

+

 

+

+

+

+

+

Bursera sp. 1

+

 

+

+

+

+

+

 

+

 

+

 

Buxaceae

Buxus bartlettii

+

+

 

+

 

+

+

+

 

+

+

+

Cecropiaceae

Cecropia peltata

+

+

+

+

+

+

+

+

+

+

+

+

Combretaceae

Bucida spinosa

    

+

       

Conocarpus erecta

      

+

     

Convolvulaceae

Evolvulus alsinoides

         

+

+

+

Ipomoea sp. 1

          

+

 

Ipomoea sp. 2

+

         

+

+

Ipomoea sp. 3

+

         

+

 

Ipomoea sp. 4

+

           

Jacquemontia nodiflora

          

+

 

Jacquemontia aff. pentantha

+

           

Merremia cisoides

        

+

  

+

Merremia tuberosa

+

+

          

Operculina pinnatifida

          

+

+

Cucurbitaceae

            

Cayaponia sp. 1

       

+

+

+

+

 

Cucurbita maxima

        

+

   

Cyperaceae

            

Rhynchospora microcarpa

 

+

    

+

+

+

+

+

+

Cyperaceae 1

        

+

+

+

 

Cyperaceae 3

         

+

  

Euphorbiaceae

            

Croton campechianus

         

+

  

Croton chichenensis

      

+

   

+

+

Croton sp. 1

+

+

    

+

   

+

+

Croton sp. 2

   

+

    

+

   

Euphorbia sp. 1

     

+

+

     

Euphorbia sp. 2

      

+

+

+

 

+

+

Euphorbia sp. 3

       

+

    

Euphorbiaceae 1

      

+

     

Fabaceae

            

Bauhinia divaricata

          

+

 

Bauhinia herrerae

          

+

+

Caesalpinia gaumeri

 

+

+

 

+

       

Caesalpinia sp. 1

 

+

        

+

 

Caesalpinia sp. 3

       

+

    

Gliricidia sepium

     

+

      

Leucaena leucocephala

+

+

+

+

    

+

+

+

+

Lonchocarpus rugosus

+

      

+

+

+

+

 

Lonchocarpus sp. 1

  

+

+

        

Lonchocarpus sp. 2

 

+

+

+

+

+

    

+

 

Lysiloma latisiliquum

    

+

+

      

Mimosa bahamensis

+

+

+

+

+

   

+

+

+

+

Mimosa pudica

+

+

 

+

    

+

+

+

+

Nissolia fruticosa

  

+

+

     

+

+

 

Piscidia piscipula

    

+

+

      

Pithecellobium albicans

      

+

     

Pithecellobium dulce

       

+

    

Stylosanthes humilis

           

+

Fabaceae 1

     

+

      

Fabaceae 2

          

+

 

Flacourtiaceae

            

Casearia nitida

     

+

      

Laetia thamnia

      

+

     

Samyda yucatanensis

+

 

+

+

+

   

+

 

+

+

Labiatae

            

Hyptis pectinata

        

+

   

Hyptis sp. 1

           

+

Leonotis nepetaefolia

           

+

Ocimum micranthum

    

+

       

Labiatae 1

        

+

   

Lauraceae

            

Nectandra coriacea

         

+

  

Loranthaceae

            

Psittacanthus mayanus

         

+

  

Malpighiaceae

            

Malpighia emarginata

         

+

+

 

Malpighia glabra

         

+

  

Malvaceae

            

Abutilon permolle

+

+

      

+

+

+

+

Hampea trilobata

        

+

   

Hibiscus sp. 1

       

+

+

+

+

 

Hibiscus sp. 2

       

+

+

+

+

+

Malvaceae 2

        

+

  

+

Moraceae

            

Chlorophora tinctoria

+

+

+

      

+

+

+

Moraceae 1

       

+

+

   

Myrtaceae

            

Calyptranthes millspaughii

+

           

Eugenia mayana

         

+

+

 

Eugenia sp. 1

+

+

+

+

+

+

+

+

+

+

+

+

Eugenia sp. 2

         

+

+

 

Eugenia sp. 3

      

+

+

  

+

 

Myrcianthes fragans

 

+

     

+

+

 

+

+

Psidium sartorianum

  

+

+

+

+

+

 

+

+

+

+

Poaceae

            

Chloris sp. 1

       

+

+

+

+

 

Eragrostis sp. 1

 

+

+

+

        

Panicum sp. 1

+

+

      

+

+

+

+

Panicum sp. 2

         

+

+

 

Panicum sp. 3

           

+

Paspalum sp. 1

       

+

+

+

+

 

Zea mays

        

+

+

  

Polygonaceae

            

Coccoloba sp. 1

      

+

+

+

+

+

 

Coccoloba sp. 2

      

+

+

  

+

+

Gymnopodium floribundum

      

+

+

+

+

+

+

Ranunculaceae

            

Clematis dioica

  

+

+

+

+

      

Rhamnaceae

            

Colubrina arborescens

          

+

 

Rubiaceae

            

Asemnanthe pubescens

      

+

+

    

Chiococca alba

      

+

    

+

Exostema caribaeum

       

+

    

Guettarda combsii

   

+

        

Rutaceae

            

Esenbeckia berlandieri

       

+

   

+

Sapindaceae

            

Exothea diphylla

           

+

Paullinia sp. 1

+

 

+

 

+

 

+

+

+

 

+

+

Serjania racemosa

+

           

Serjania yucatanensis

 

+

+

+

     

+

+

+

Serjania sp. 2

      

+

     

Serjania sp. 4

          

+

 

Thouinia canesceras

+

+

+

+

 

+

+

+

+

+

+

+

Sapindaceae 1

       

+

    

Sapotaceae

            

Bumelia sp. 1

          

+

 

Pouteria mammosa

           

+

Pouteria sp. 1

+

+

+

+

+

+

  

+

+

+

+

Pouteria sp. 2

  

+

+

+

   

+

+

+

 

Sapotaceae 1

+

     

+

   

+

 

Sapotaceae 2

           

+

Sapotaceae 3

         

+

  

Scrophulariaceae

            

Capraria biflora

        

+

   

Smilacaceae

            

Smilax spinosa

 

+

+

         

Tiliaceae

            

Corchorus sp. 1

           

+

Heliocarpus donnell-smithii

           

+

Heliocarpus sp. 1

+

         

+

 

Heliocarpus sp. 2

           

+

Luehea speciosa

           

+

Triumfetta dumetorum

+

+

          

Ulmaceae

            

Trema micrantha

+

+

+

+

 

+

+

+

+

+

+

+

Vervenaceae

            

Verbenaceae 1

       

+

    

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Villanueva-Gutiérrez, R., Roubik, D.W., Porter-Bolland, L. (2015). Bee–Plant Interactions: Competition and Phenology of Flowers Visited by Bees. In: Islebe, G., Calmé, S., León-Cortés, J., Schmook, B. (eds) Biodiversity and Conservation of the Yucatán Peninsula. Springer, Cham. https://doi.org/10.1007/978-3-319-06529-8_6

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