Landscape Structure Effects on Bee and Wasp Assemblages in a Semiarid Buffer Zone

  • Lilian Maria Araujo Flores Federal University of Ceará – UFC, Department of Biology, Graduate Course of Ecology and Natural Resources, Fortaleza-Ceará, Brazil
  • Lorenzo Roberto Sgobaro Zanette Federal University of Ceará – UFC, Department of Biology, Graduate Course of Ecology and Natural Resources, Fortaleza-Ceará, Brazil
  • Danilo Boscolo University of São Paulo - USP, Faculty of Philosophy, Sciences and Letters of Ribeirão Preto - FFCLRP, Department of Biology, São Paulo, Brazil
  • Francisca Soares Araújo Federal University of Ceará – UFC, Department of Biology, Graduate Course of Ecology and Natural Resources, Fortaleza-Ceará, Brazil
Keywords: Landscape change, Agroecosystem, Ecosystem services, Trap-nest, Dry forest


Understanding the effects of anthropogenic changes on groups that perform key ecosystem services, such as pollination and pest control, is essential for conservation and maintenance of these groups in landscapes. We aimed to understand how landscape heterogeneity and the natural vegetation loss affect the diversity of bees, wasps and their parasitoids in a resource limited semiarid environment. We sampled bees and wasps that nest in pre-existing cavities in 20 landscapes, for two years, in Ubajara National Park, in northeastern of Brazil. We recorded eleven species of bees, nine of wasps and six of parasitoids in 657 trapnests. Landscape heterogeneity had different effects on bees, wasps and their parasitoids. Landscape configuration had stronger effect than composition. Bee abundance decreased according to the complexity of the spatial arrangement of landscape units, while wasp abundance increased. Our study shows that in semiarid regions some species may have different responses to landscape structure from those found in other regions. The spatial patterns described here have important implications for conservation of these essential biological groups, indicating that conservation actions for these groups should associate both landscape composition and configuration to increase the provision of resources and to facilitate the access to resources throughout the year.


Abrahamczyk, S.; Kluge, J.; Gareca, Y.; Reichle, S. & Kessler, M. 2011. The influence of climatic seasonality on the diversity of different tropical pollinator groups. PLoS ONE 6(11), 1-9. DOI:10.1371/journal.pone.0027115

Aguiar, C.M.L.; Garófalo, C.A. & Almeida, G.F. 2005. Trap-nesting bees (Hymenoptera, Apoidea) in areas of dry semideciduous forest and caatinga, Bahia, Brazil. Revista Brasileira de Zoologia 22, 1030-1038. DOI:10.1590/S0101-81752005000400031

Antongiovanni, M. & Metzger, J.P. 2005. Influence of matrix habitats on the occurrence of insectivorous bird species in Amazonian forest fragments. Biological Conservation 122(3), 441-451. DOI:10.1016/j.biocon.2004.09.005

Araujo, F.S.; Menezes, M.O.T.; Barbosa, L.S.; Oliveira, V.M.R.; Nogueira Rafaella, S.; Menezes, B.S.; Souza, B.C.; Carvalho, E.C.D.; Silveira, A.P.; Flores, L.M.A. & Zanette, L.R.S. 2017. Efetividade da zona de amortecimento de unidades de conservação federais do estado do Ceará: Parque Nacional de Ubajara e Estação Ecológica de Aiuaba. In: W. Mantovani, R.F. Monteiro, L. Anjos & M.O. Cariello (eds.): Pesquisas em unidades de conservação no domínio da caatinga: subsídios à gestão. Edições UFC – Fortaleza.

Araújo, F.S.; Rodal, M.J.N.; Barbosa, M.R.V. & Martins, F.R. 2005. Repartição da flora lenhosa no domínio da Caatinga. In: F.S. Araújo, Rodal, M.J.N. & Barbosa, M.R.V. (eds.): Análise das Variações da Biodiversidade do Bioma Caatinga: Suporte a Estratégias Regionais de Conservação. Ministério do Meio Ambiente – Brasília.

Ashman, T.L.; Knight, T.M.; Steets, J.A.; Amarasekare, P.; Burd, M.; Campbell, D.R. & Wilson, W.G. 2004. Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85(9), 2408–2421. DOI:10.1890/03-8024

Barton, K. 2019. MuMIn: Multi-Model Inference. R package version 1.43.6. https://CRAN.R-project. org/package=MuMIn (Date: 20.06.2019)

Batra, S.W. 1984. Solitary bees. Scientific American, 250, 86-93. DOI:10.1038/scientificamerican0284-120

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

Burnham, K.P. & Anderson, D.R. 2002. Model selection and multimodel inference: a practical information-theoretic approach. second ed., Springer, New York, USA.

Buschini, M.L.T. & Wolff, L.L. 2006. Notes on the biology of Trypoxylon (Trypargilum) opacum Brèthes (Hymenoptera; Crabronidae) in southern Brazil. Brazilian Journal of Biology 66(3), 907-917. DOI:10.1590/S1519-69842006000500017

Câmara, G.; Souza, R.C.M.; Freitas, U.M. & Garrido, J. 1996. SPRING - Integrating remote sensing and GIS by object-oriented data modelling. Computers & Graphics 20, 395-403. DOI:10.1016/0097-8493(96)00008-8

Chapin III, F.S.; Zavaleta, E.S.; Eviner, V.T.; Naylor, R.L.; Vitousek, P.M.; Reynolds, H.L. & Díaz, S. 2000. Consequences of changing biodiversity. Nature 405(6783), 234-242. DOI:10.1038/35012241

Charman, T.G.; Sears, J.; Green, R.E. & Bourke, A.F. 2010. Conservation genetics, foraging distance and nest density of the scarce Great Yellow Bumblebee (Bombus distinguendus). Molecular Ecology 19(13), 2661-2674. DOI:10.1111/j.1365- 294X.2010.04697.x

Dale, V.H.; Brown, S.; Haeuber, R.A.; Hobbs, N.T.; Huntly, N.; Naiman, R.J.; Riebsame, W.E.; Turner, M.G. & Valone, T.J. 2000. Ecological principles and guidelines for managing the use of land. Ecological Applications 10(3), 639-670. DOI:10.1890/1051-0761(2000)010[0639:EPAGFM]2.0.CO;2

Didham, R.K.; Ghazoul, J.; Stork, N.E. & Davis, A.J. 1996. Insects in fragmented forests: a functional approach. Trends in Ecology & Evolution 11, 255- 60. DOI:10.1016/0169-5347(96)20047-3

Dingle, H. & Drake, V.A. 2007. What is migration? BioScience 57(2), 113-121. DOI:10.1641/B570206

Ebeling, A.; Klein, A.M.; Weisser, W.W. & Tscharntke, T. 2012. Multitrophic effects of experimental changes in plant diversity on cavity-nesting bees, wasps, and their parasitoids. Oecologia 169, 453- 65. DOI:10.1007/s00442-011-2205-8

Fabian, Y.; Sandau, N.; Bruggisser, O.T.; Aebi, A.; Kehrli, P.; Rohr, R.P.; Naisbit, R.E. & Bersier, L.F. 2013. The importance of landscape and spatial structure for hymenopteran-based food webs in an agro-ecosystem. Journal of Animal Ecology 82, 1203–1214. DOI:10.1111/1365-2656.12103

Fahrig, L. 2017. Ecological responses to habitat fragmentation per se. Annual Review of Ecology, Evolution, and Systematics 48(1), 1-23. DOI:10.1146/annurev-ecolsys-110316-022612

Fahrig, L.; Baudry, J.; Brotons, L.; Burel, F.G.; Crist, T.O.; Fuller, R.J.; Sirami, C.; Siriwardena, G.M. & 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

Fahrig, L.; Girard, J.; Duro, D.; Pasher, J.; Smith, A.; Javorek, S. & Tischendorf, L. 2015. Farmlands with smaller crop fields have higher within- field biodiversity. Agriculture, Ecosystems & Environment 200, 219-234. DOI:10.1016/j. agee.2014.11.018

Falk, S. & Lewington, R. 2015. Field Guide to the Bees of Great Britain and Ireland. British Wildlife Publishing Lt. – London.

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

Figueiredo, M.A. 1988. As serras úmidas no Ceará e a produção alimentar para o semi-árido cearense. Coleção Mossoroense 353, 1-15.

Flores, L.M.A.; Zanette, L.R.S. & Araújo, F.S. 2018. Effects of habitat simplification on assemblages of cavity nesting bees and wasps in a semiarid neotropical conservation area. Biodiversity and Conservation 27, 311–328. DOI:10.1007/s10531-017-1436-3

Franklin, J.F. & Forman, R.T. 1987. Creating landscape patterns by forest cutting: ecological consequences and principles. Landscape Ecology 1(1), 5-18. DOI:10.1007/BF02275261

Fricke, J.M. 1991. Trap-nest bore diameter preferences among sympatric Passaloecus spp. (Hymenoptera: Spheci¬dae). Great Lakes Entomology 24, 123-125.

FUNCEME 2015. Fundação Cearense de Meteorologia e Recursos Hídricos. http:/www. (Date: 03.05.2015).

Fye, R.E. 1972. The effect of forest disturbances on populations of wasps and bees in northwestern Ontario (Hymenoptera: Aculeata). The Canadian Entomologist 104(10), 1623-1633. DOI:10.4039/ Ent1041623-10

Gallai, N.; Salles, J.M.; Settele, J. & Vaissière, B.E. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological economics 68(3), 810-821. DOI:10.1016/j.ecolecon.2008.06.014

Gathmann, A. & Tscharntke, T. 2002. Foraging ranges of solitarybees. Journalof Animal Ecology 71, 757– 764. DOI:10.1046/j.1365-2656.2002.00641.x

Goodell, K. 2003. Food availability affects Osmia pumila (Hymenoptera: Megachilidae) foraging, reproduction, and brood parasitism. Oecologia 134(4), 518-527. DOI:10.1007/s00442-002-1159-2

Gould, W.P. & Jeanne, R.L. 1984. Polistes wasps (Hymenoptera: Vespidae) as control agents for lepidopterous cabbage pests. Environmental Entomology 13, 150–56. DOI:10.1093/ ee/13.1.150

Happe, A.K.; Riesch, F.; Rösch, V.; Gallé, R.; Tscharntke, T. & Batáry, P. 2018. Small-scale agricultural landscapes and organic management support wild bee communities of cereal field boundaries. Agriculture, Ecosystems & Environment 254, 92– 98. DOI:10.1016/j.agee.2017.11.019

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

Hoffmann, U.S.; Jauker, F.; Lanzen, J.; Warzecha, D.; Wolters, V. & Diekötter, T. 2018. Prey-dependent benefits of sown wildflower strips on solitary wasps in agroecosystems. Insect Conservation and Diversity 11, 42–49. DOI:10.1111/icad.12270

Holzschuh, A.; Steffan-Dewenter, I. & Tscharntke, T. 2010. How do landscape composition and configuration organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids? Journal of Animal Ecology 79(2), 491– 500. DOI:10.1111/j.1365-2656.2009.01642.x

Jennings, D.T. & Houseweart, M.W. 1984. Predation by eumenid wasps (Hymenoptera: Eumenidae) on spruce budworm (Lepidoptera: Tortricidae) and other lepidopterous larvae in spruce-fir forests of Maine. Annals of the Entomological Society of America 77(1), 39-45. DOI:10.1093/aesa/77.1.39

Kennedy, C.; Lonsdorf, E.; Neel, M.C.; Williams, N.M.; Ricketts, T.H.; Winfree, R.; Bommarco, R.; Brittain, C.; Burley, A.L.; Cariveau, D.; Carvalheiro, L.G.; Chacoff, N.P.; Cunningham, S.A.; Danforth, B.N.; Dudenhöffer, J.; Elle, E.; Gaines, H.R.; Garibaldi, L.A.; Gratton, C.; Holzschuh, A.; Isaacs, R.; Javorek, S.K.; Jha, S.; Klein, A.M.; Krewenka, K.; Mandelik, Y.; Mayfield, M.M.; Morandin, L.; Neame, L.A.; Otieno, M.; Park, M.; Potts, S.G.; Rundlöf, M.; Saez, A.; Steffan-Dewenter, I.; Taki, H.; Viana, B.F.; Westphal, C.; Wilson, J.K.; Greenleaf, S.S. & Kremen, C. 2013. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecology Letters 16(5), 584–599. DOI:10.1111/ele.12082

Klein, A.M.; Steffan-Dewenter, I. & Tscharntke, T. 2004. Foraging trip duration and density of megachilid bees, eumenid wasps and pompilid wasps in tropical agroforestry systems. Journal of Animal Ecology 73, 517–525. DOI:10.1111/j.0021- 8790.2004.00826.x

Klein, A.M.; Steffan-Dewenter, I.; Buchori, D. & Tscharntke, T. 2002. Effects of land-use intensity in tropical agroforestry systems on flower-visiting and trap-nesting bees and wasps. Conservation Biology 16(4), 1003–1014. DOI:10.1046/j.1523- 1739.2002.00499.x

Klein, A.M.; Vaissière, B.E.; Cane, J.H.; Steffan- Dewenter, I.; Cunningham, S.A.; Kremen, C. & Tscharntke T. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274: 303-13, 2007. DOI:10.1098/rspb.2006.3721

Krewenka, K.M.; Holzschuh, A.; Tscharntke, T. & Dormann, C.F. 2011. Landscape elements as potential barriers and corridors for bees, wasps and parasitoids. Biological Conservation 144(6), 1816-1825. DOI:10.1016/j.biocon.2011.03.014

Krombein, K.V. 1967. Trap-nesting wasps and bees: life histories, nests, and associates. Smithsonian Press – Washington DC.

Loyola, R.D. & Martins, R.P. 2008. Habitat structure components are effective predictors of trap- nesting Hymenoptera diversity. Basic and Applied Ecology 9, 735-742. DOI:10.1016/j. baae.2007.06.016

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.

Melo, R.R. & Zanella, F.C. 2012. Dinâmica de fundação de ninhos por abelhas e vespas solitárias (Hymenoptera, Aculeta) em área de caatinga na Estação Ecológica do Seridó. Revista Brasileira de Ciências Agrárias 7, 657-662. DOI:10.5039/ agraria.v7i4a1966

Metzger, J.P. 2001. O que é ecologia de paisagens? Biota Neotropica 1, 1-9. DOI:10.1590/S1676-06032001000100006

Morandin, L.A. & Winston, M.L. 2006. Pollinators provide economic incentive to preserve natural land in agroecosystems. Agriculture, Ecosystems & Environment 116(3), 289-292. DOI:10.1016/j. agee.2006.02.012

Morato, E.F. & Martins, R.P. 2006. An overview of proximate factors affecting the nesting behavior of solitary wasps and bees (Hymenoptera: Aculeata) in preexisting cavities in wood. Neotropical Entomology 35(3), 285-98. DOI:10.1590/S1519- 566X2006000300001

Moreira, E.F.; Boscolo, D. & Viana, B.F. 2015. Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS ONE 10(4), e0123628. DOI:10.1371/journal.pone.0123628

Nascimento, A.L.O. & Garófalo, C.A. 2014. Trap- nesting solitary wasps (Hymenoptera: Aculeata) in an insular landscape: Mortality rates for immature wasps, parasitism, and sex ratios. Sociobiology 61(2), 207-217. DOI:10.13102/ sociobiology.v61i2.207-217

Nether, M.C.; Dudek, J., & Buschini, M.L.T. 2019. Trophic interaction and diversity of cavity-nesting bees and wasps (Hymenoptera: Aculeata) in Atlantic forest fragments and in adjacent matrices. Apidologie 50(1), 104-115. DOI:10.1007/s13592- 018-0623-x

O‘Neill, K.M. 2001. Solitary wasps: behavior and natural history. Cornell University Press – Ithaca.

Pardini, R.; Bueno, A.A.; Gardner, T.A.; Prado, P.I. & Metzger, J.P. 2010. Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS ONE 5(10), e13666. DOI:10.1371/journal.pone.0013666

Penagos, D.I. & Williams, T. 1995. Important factors in the biology of heteronomous hyperparasitoids (Hym: Aphelinidae): Agents for the biological control of whiteflies and scale insects. Acta Zoológica Mexicana 66, 31–57.

Pereira-Peixoto, M.H.; Pufal, G.; Martins, C.F. & Klein, A.M. 2014. Spillover of trap-nesting bees and wasps in an urban–rural interface. Journal of Insect Conservation 18(5), 815-826. DOI:10.1007/ s10841-014-9688-7

Perfecto, I.; Vandermeer, J. & Wright, A. 2009. Nature’s matrix: linking agriculture, conservation and food sovereignty. Earthscan – London.

Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O. & Kunin, W.E. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25(6), 345-353. DOI:10.1016/j.tree.2010.01.007

R Core Team 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing – Vienna. URL https://www.R-project. org/ (Date: 20.06.2019)

Ricketts, T.H. 2001. The matrix matters: effective isolation in fragmented landscapes. The American Naturalist 158(1), 87-99. DOI:10.1086/320863

Ricketts, T.H.; Regetz, J.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Bogdanski, A.; Gemmill-Herren, B.; Greenleaf, S.S.; Klein, A.M.; Mayfield, M.M.; Morandin, L.A.; Ochieng,

A. & Viana, B.F. 2008. Landscape effects on crop pollination services: are there general patterns? Ecology Letters 11(5), 499–515. DOI:10.1111/j.1461-0248.2008.01157.x

Rodal, M.J.N.; Sales, M.F.; Silva, M.J. & Silva, A.G. 2005. Flora de um Brejo de Altitude na escarpa oriental do planalto da Borborema, PE, Brasil. Acta Botanica Brasilica 19(4), 843-858. DOI:10.1590/S0102-33062005000400020

Roubik, D.W. 2001. Ups and downs in pollinator populations: whenisthereadecline? Conservation Ecology 5, 1-22.

Rubene, D.; Schroeder, M. & Ranius, T. 2015. Diversity patterns of wild bees and wasps in managed boreal forests: effects of spatial structure, local habitat and surrounding landscape. Biological Conservation 184, 201-208. v

Schmidt, M.H.; Roschewitz, I.; Thies, C. & Tscharntke, T. 2005. Differential effects of landscape and management on diversity and density of ground- dwelling farmland spiders. Journal of Applied Ecology 42(2), 281-287. DOI:10.1111/j.1365- 2664.2005.01014.x

Schüepp, C.; Herrmann, J.D.; Herzog, F. & Schmidt- Entling, M.H. 2011. Differential effects of habitat isolation and landscape composition on wasps, bees, and their enemies. Oecologia 165(3), 713– 721. DOI:10.1007/s00442-010-1746-6

Schwinning, S.; Sala, O.E.; Loik, M.E. & Ehleringer, J.R. 2004. Thresholds, memory, and seasonality: understanding pulse dynamics in arid/semi-arid ecosystems. Oecologia 141(2), 191–193. DOI:10.1007/s00442-004-1683-3

Steckel, J.; Westphal, C.; Peters, M.K.; Bellach, M.; Rothenwoehrer, C.; Erasmi, S.; Scherber, C.; Tscharntke, T. & Steffan-Dewenter, I. 2014. Landscape composition and configuration differently affect trap-nesting bees, wasps and their antagonists. Biological Conservation 172, 56-64. DOI:10.1016/j.biocon.2014.02.015

Symondson, W.O.C.; Sunderland, K.D. & Greenstone, H.M. 2002. Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47, 561–594. DOI:10.1146/annurev. ento.47.091201.145240

Taki, H.; Viana, B.F.; Kevan, P.G.; Silva, F.O. & Buck, M. 2008. Does forest loss affect the communities of trap-nesting wasps (Hymenoptera: Aculeata) in forests? Landscape vs. local habitat conditions. Journal of Insect Conservation 12(1), 15-21. DOI:10.1007/s10841-006-9058-1

Thies, C.; Steffan-Dewenter, I. & Tscharntke, T. 2003. Effects of landscape context on herbivory and parasitism at different spatial scales. Oikos 101(1), 18-25. DOI:10.1034/j.1600-0706.2003.12567.x

Thornthwaite, C.W. 1948. An approach toward a rational classification of climate. Geographical Review 38, 55–94. DOI:10.2307/210739

Tscharntke, T.; Gathmann, A. & Steffan-Dewenter, I. 1998. Bioindication using trap-nesting bees and wasps and their natural enemies. Journal of Applied Ecology 35(5), 708-719. DOI:10.1046/j.1365-2664.1998.355343.x

Tylianakis, J.M.; Klein, A.M. & Tscharntke, T. 2005. Spatiotemporal variation in the diversity of hymenoptera across a tropical habitat gradient. Ecology 86(12), 3296-3302. DOI:10.1890/05-0371

Venables, W.N. & Ripley, B.D. 2002. Modern Applied Statistics with S. Fourth Edition. Springer – NewYork.

Williams, N.M. & Kremen, C. 2007. Resource distributions among habitats determine solitary bee offspring production in a mosaic landscape. Ecological Applications 17(3), 910–921. DOI:10.1890/06-0269

Winfree, R.; Griswold, T. & Kremen, C. 2007. Effect of human disturbance on bee communities in a forested ecosystem. Conservation Biology 21(1), 213-223. DOI:10.1111/j.1523-1739.2006.00574.x

Zurbuchen, A.; Landert, L.; Klaiber, J.; Müller, A.; Hein, S. & Dorn, S. 2010. Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biological Conservation 143(3), 669–676. DOI:10.1016/j.biocon.2009.12.003

Title LO.201976
How to Cite
Flores, L. M. A.; Zanette, L. R. S.; Boscolo, D.; Araújo, F. S. Landscape Structure Effects on Bee and Wasp Assemblages in a Semiarid Buffer Zone. LO 2019, 76, 1-17.
Research Article