Bee diversity responses to forest and open areas in heterogeneous Atlantic Forest

Authors

  • Laura Silva Nery Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto - Universidade de São Paulo
  • Juliana Toshie Takata Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto - Universidade de São Paulo
  • Bruna Bertagni de Camargo Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto - Universidade de São Paulo.
  • Aryel Moreno Chaves Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto - Universidade de São Paulo
  • Patrícia Alves Ferreira Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Universidade de São Paulo. Departamento de Ciências Ambientais, Universidade Federal de São Carlos.
  • Danilo Boscolo Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto - Universidade de São Paulo

DOI:

https://doi.org/10.13102/sociobiology.v65i4.3472

Keywords:

Pollination, landscape complementation, Atlantic Forest, landscape heterogeneity, Brazil.

Abstract

Agriculture driven landscape changes has caused worldwide forest loss and fragmentation, seriously affecting biodiversity and ecosystem services, amongst which pollination is remarkably important. Bees are an essential pollinator group for forest plant populations and food production in tropical landscapes. They are also dependent on forested environments which are essential to maintain their diversity and pollination services. We analyzed bee diversity in contrasting forest and adjacent non-forest patches to evaluate if bees can use complementary non-native environments in heterogeneous altered tropical landscapes. The effect of landscape level heterogeneity and forest amount on bee diversity was also assessed. Our hypothesis was that bee communities would be more rich and diverse inside the forest understory, but due to supplementary foraging behaviors they would be more abundant in non-forested areas where flower availability is higher. We actively sampled bees visiting flowers within forest patches and in surrounding non-forest open areas between the Cantareira and Mantiqueira mountain ranges in São Paulo, Brazil. We found higher bee richness and diversity in open areas than in forest patches, partially denying our initial hypothesis but supporting that bees are more abundant in non-forest areas. We found strong indication that landscapes with higher amount of forest and environmental heterogeneity can provide more resources for bees through resource complementation processes, maintaining their diversity in the landscape. The presence of forest patches close to crop and open areas is of utmost importance for the conservation of bees and pollination services with important consequences for land management in tropical environments.

Downloads

Plum Print visual indicator of research metrics
  • Citations
  • Scopus - Citation Indexes: 27
  • Captures
  • Mendeley - Readers: 87
-
see details

References

Aizen, M. A. & Feinsinger, P. (1994). Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine 'Chaco

Serrano'. Ecological applications, 4(2): 378-392 doi:10.2307/1941941.

Aizen, M. A., Morales, C. L. & Morales, J. M. (2008). Invasive mutualists erode native pollination webs. PLoS biology, 6(2): 0397-0403. doi:10.1371/journal.pbio.0060031.

Andren, H. (1994). Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos, 71: 355-366 doi:10.2307/3545823.

Asner, G. P., Elmore, A. J., Olander, L. P., Martin, R. E. & Harris, A.

T. (2004). Grazing systems, ecosystem responses, and global change. Annu. Rev. Environ. Resour, 29: 261-299. doi:10.1146/annurev.energy.29.062403.102142.

Barnosky, A. D., Hadly, E. A., Bascompte, J., Berlow, E. L., Brown, J. H., Fortelius, M. & Martinez, N. D. (2012). Approaching a state shift in Earth’s biosphere. Nature, 486(7401): 52–58. doi:10.1038/nature11018.

Baudena, M., Dekker, S. C., van Bodegom, P. M., Cuesta, B., Higgins, S. I., Lehsten, V. & Zavala, M. A. (2015). Forests, savannas and grasslands: bridging the knowledge gap between ecology and Dynamic Global Vegetation Models. Biogeosciences, 12: 1833–1848,. doi:10.5194/bg-12-1833-2015 .

Bawa, K. S. (1990). Plant-pollinator interactions in tropical rain forests. Annual review of Ecology and Systematics, 21 :399-422. doi:10.1146/annurev.es.21.110190.002151

Bergin, T. M., Best, L. B., Freemark, K. E. & Koehler, K. J. (2000). Effects of landscape structure on nest predation in roadsides of a midwestern agroecosystem: a multiscale analysis. Landscape Ecology, 15(2): 131-143. doi:10.1023/A:1008112825655.

Boscolo, D., Tokumoto, P. M., Ferreira, P. A., Ribeiro, J. W. & Santos, J. S. (2017). Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels. Perspectives in Ecology and Conservation, 15: 18-24 doi: 10.1016/j.pecon.2017.03.002

Brosi, B. J., Armsworth, P. R. & Daily, G. C. (2008). Optimal design of agricultural landscapes for pollination services. Conservation Letters, 1: 27-36. doi:10.1111/j.1755-263X.2008.00004.x

Brosi, B. J. (2009). The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biological Conservation, 142(2): 414-423. doi: 10.1016/j.biocon.2008.11.003

Carvalheiro, L. G., Seymour, C. L., Veldtman, R. & Nicolson, S. W. (2010). Pollination services decline with distance from natural habitat even in biodiversity‐rich areas. Journal of Applied Ecology, 47(4): 810-820. doi:10.1111/j.1365-2664.2010.01829.x

Chacoff, N. P. & Aizen, M. A. (2006). Edge effects on flower‐visiting insects in grapefruit plantations bordering premontane subtropical forest. Journal of Applied Ecology, 43: 18-27.doi: 10.1111/j.1365-2664.2005.01116.x

Dean, W., & Ferro, A. (1996). Fogo: a história e a devastação da Mata Atlântica. São Paulo, Companhia das Letras, 23 p.

Dunning, J. B., Danielson, B. J. & Pulliam, H. R. (1992). Ecological processes that affect populations in complex landscapes. Oikos, 65: 169-175. doi:10.2307/3544901

Eilers, E. J., Kremen, C., Greenleaf, S. S., Garber, A. K. & Klein, A. M. (2011). Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS one, 6(6): 1-6. doi: 10.1371/journal.pone.0021363

Fahrig, L. (1998). When does fragmentation of breeding habitat affect population survival?. Ecological Modelling, 105(2-3): 273-292. doi:10.1016/S0304-3800(97)00163-4

Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual review of ecology, evolution, and systematics, 34: 487-515 . doi:10.1146/annurev.ecolsys.34.011802.132419

Fahrig, L., Baudry, J., Brotons, L., Burel, F. G., Crist, T. O., Fuller, R. J.& Martin, J. L. (2011). Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecology letters, 14(2): 101-112. doi:10.1111/j.1461-0248.2010.01559.x

Ferreira, J., Pardini, R., Metzger, J.P. & Fonseca, C. R. (2012). Towards environmentally sustainable agriculture in Brazil: challenges and opportunities for applied ecological research. Journal of applied Ecology 49(3): 535-541. doi: 10.1111/j.1365-2664.2012.02145.x

Ferreira, P. A., Boscolo, D., Carvalheiro, L. G., Biesmeijer, J. C., Rocha, P. L. & Viana, B. F. (2015). Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic Rainforest. Landscape ecology, 30(10): 2067–2078. doi:10.1007/s10980-015-0231-3

Gibbs, H. K., Ruesch, A. S., Achard, F., Clayton, M. K., Holmgren, P., Ramankutty, N. & Foley, J. A. (2010). Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proceedings of the National Academy of Sciences, 107(38): 16732-16737. doi: 10.1073/pnas.0910275107

Hilário, S. D., Imperatriz-Fonseca, V. L. & Kleinert, A. D. M. P. (2001). Responses to climatic factors by foragers of Plebeia pugnax Moure (in litt.)(Apidae, Meliponinae). Revista Brasileira de Biologia, 61(2): 191-196. . doi: 10.1590/S0034-71082001000200003

Hipólito, J., Boscolo, D. & Viana, B. F. (2018). Landscape and crop management strategies to conserve pollination services and increase yields in tropical coffee farms. Agriculture, Ecosystems & Environment, 256: 218-225. doi: 10.1016/j.agee.2017.09.038

IBGE - Instituto Brasileiro de Geografia e Estatística. (1992). Manual técnico da vegetação brasileira. Manuais Técnicos em Geociências, Vol. 1, 16.

Jaeger, T. (2005). Nuevas perspectivas para el programa MAB y las reservas de Biosfera. Lecciones aprendidas en América. UNESCO. División de Ciencias Ecológicas y de la Tierra. Programa de Cooperación Sur-Sur. Documento de Trabajo Nº 35.

Jha, S. & Vandermeer, J. H. (2010). Impacts of coffee agroforestry management on tropical bee communities. Biological Conservation, 143(6): 1423-1431. doi: 10.1016/j.biocon.2010.03.017

Klein, A. M., Vaissiere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B: Biological Sciences, 274(1608):303-313. doi:10.1098/rspb.2006.3721

Lambin, E. F., Turner, B. L., Geist, H. J., Agbola, S. B., Angelsen, A., Bruce, J. W.... & George, P. (2001). The causes of land-use and land-cover change: moving beyond the myths. Global environmental change, 11(4): 261-269. doi: 10.1016/S0959-3780(01)00007-3

Landy, M.K., Roberts, M.J. & Thomas, S.R. 1990. The environmental protection agency - asking the wrong questions. United States: N. p. Web.

Lindgren, J., Kimberley, A., Eriksson, O. & Cousins, S. (2017). Habitat complementary supports pollinators and frugivores in agricultural landscapes. Retrieved from http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-148650

McGarigal, K., Cushman, S.A., & Ene, E. (2012). FRAGSTATS v4: Spatial Pattern Analysis Program for Categorical and Continuous Maps. Computer software program produced by the authors at the University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html (accessed date: 10 May, 2018)

Morato, E. F., Garcia, M. V. & Campos, L. A. D. O. (1999). Biologia de Centris Fabricius (Hymenoptera, Anthophoridae, Centridini) em matas contínuas e fragmentos na Amazônia Central. Revista Brasileira de Zoologia, 16(4): 1213-1222. doi: 10.1590/S0101-81751999000400029

Moreira, E. F., Boscolo, D. & Viana, B. F. (2015). Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PloS one, 10(4): 1-19. doi: 10.1371/journal.pone.0123628

Moreira, E. F., Santos, R. L. S., Silveira, M. S. & Boscolo, D. (2017). Influence of landscape structure on Euglossini composition in open vegetation environments. Biota Neotropica 17: 1-7. doi: :10.1590/1676-0611-bn-2016-0294

Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature,403: 853–858. doi:10.1038/35002501

Nielsen, A. & Bascompte, J. (2007). Ecological networks, nestedness and sampling effort. Journal of Ecology, 95(5): 1134-1141. doi: 10.1111/j.1365-2745.2007.01271.x

Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D, Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E. & Wagner, H. (2017) vegan: community ecology package in R package version 2.4‐0.

Pearson, S. M. (1993). The spatial extent and relative influence of landscape-level factors on wintering bird populations. Landscape Ecology, 8(1), 3-18. doi: 10.1007/BF00129863.

Potts, S. G., Imperatriz-Fonseca, V., Ngo, H. T., Aizen, M. A., Biesmeijer, J. C., Breeze, T. D. & Vanbergen, A. J. (2016). Safeguarding pollinators and their values to human well-being. Nature, 540: 220–229. doi:10.1038/nature20588.

Ramalho, M. (2004). Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Acta Botanica Brasilica, 18(1): 37-47. doi: 10.1590/S0102-33062004000100005

Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J. & Hirota, M. M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological conservation, 142(6): 1141-1153. doi:10.1016/j.biocon.2009.02.021

Rickketts, T. H., Daily, G. C., Enrlich, P.R. & Michener, C.D. (2004). Economic value of tropical forest to coffee production. PNAS. 101 (34) 12579-12582. doi: 10.1073/pnas.0405147101

Sistema de Informações Florestais do Estado de São Paulo - SIFESP (2009). Inventário Florestal. http://www2.ambiente.sp.gov.br/sifesp/inventario-fl orestal/#. (accessed date: 8 August, 2018)

Sparovek, G., Berndes, G., Klug, I. L., & Barretto, A. G. (2010). Brazilian agriculture and environmental legislation: status and future challenges., 44(16): 6046–6053. doi: 10.1021/es1007824.

Steffan-Dewenter, I., Münzenberg, U., Bürger, C., Thies, C., & Tscharntke, T. (2002). Scale‐dependent effects of landscape context on three pollinator guilds. Ecology, 83(5): 1421-1432. doi: 10.1890/0012-9658(2002)083[1421:SDEOLC]2.0.CO;2

Team, R. (2017). RStudio: Integrated Development for R (version 1.1. 383)[Computer software].

Terborgh, J. (1985). The vertical component of plant species diversity in temperate and tropical forests. The American Naturalist, 126(6): 760-776. doi: 10.1086/284452

Tonhasca Jr, A., Albuquerque, G. S. & Blackmer, J. L. (2003). Dispersal of euglossine bees between fragments of the Brazilian Atlantic Forest. Journal of Tropical Ecology, 19(1): 99-102. doi:10.1017/S0266467403003122

Tscharntke, T., Tylianakis, J. M., Rand, T. A., Didham, R. K., Fahrig, L., Batary, P. & Ewers, R. M. (2012). Landscape moderation of biodiversity patterns and processes‐eight hypotheses. Biological Reviews, 87(3): 661-685. doi:10.1111/j.1469-185X.2011.00216.x

Van Geert, A., Van Rossum, F. & Triest, L. (2010). Do linear landscape elements in farmland act as biological corridors for pollen dispersal? Journal of Ecology, 98(1): 178-187. doi:10.1111/j.1365-2745.2009.01600.x

Veloso, H.P., Rangel Filho, A.L.R. & Lima, J.C.A. (1991). Classifi cação da vegetação Brasileira adaptada a um sistema universal. Rio de Janeiro: Instituto Brasileiro de Geografi a e Estatística.

Whately, M.; Cunha, P. (2007). Cantareira 2006 : um olhar sobre o maior manancial de água da Região Metropolitana de São Paulo. Instituto Socioambiental, São Paulo.

Wender, B. W. , Harrington, C. A. & Tappeiner, J. C. (2004). Flower and fruit production of understory shrubs in western Washington and Oregon. Northwest Science 78(2): 124-140.

Winfree, R., Williams, N. M., Gaines, H., Ascher, J. S., & Kremen, C. (2008). Wild bee pollinators provide the majority of crop visitation across land‐use gradients in New Jersey and Pennsylvania, USA. Journal of Applied Ecology, 45(3): 793-802. doi: 10.1111/j.1365-2664.2007.01418.x

Downloads

Published

2018-10-11

How to Cite

Nery, L. S., Takata, J. T., de Camargo, B. B., Chaves, A. M., Ferreira, P. A., & Boscolo, D. (2018). Bee diversity responses to forest and open areas in heterogeneous Atlantic Forest. Sociobiology, 65(4), 686–695. https://doi.org/10.13102/sociobiology.v65i4.3472

Issue

Vol. 65 No. 4 (2018)

Section

Research Article - Bees

License

Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.

Authors who publish with this journal agree to the following terms:

 

    1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

 

    1. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

 

  1. Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).

Most read articles by the same author(s)