Skip to main content

Advertisement

SpringerLink
Log in

Contrasting Patterns in Solitary and Eusocial Bees While Responding to Landscape Features in the Brazilian Cerrado: a Multiscaled Perspective

  • Ecology, Behavior and Bionomics
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

Landscape structure is an important determinant of biological fluxes and species composition, but species do not respond equally to landscape features or spatial extents. Evaluating “multi-scale” responses of species to landscape structure is an important framework to be considered, allowing insights about habitat requirements for different groups. We evaluated the response of Brazilian Cerrado’s bees (eusocial vs. solitary ones) to both the amount and isolation of remnant vegetation in eight nested multiple-local scales. Response variables included abundance, observed, and estimated species richness, and beta diversity (split into nestedness and turnover resultant dissimilarities). Eusocial species’ abundance responded to landscape structure at narrow scales of fragment isolation (250 m of radius from sampling sites), while solitary species’ abundance responded to broader scales to fragment area (2000 m). Eusocial species nestedness also responded to landscape features in broader scales (1500 m), especially to increasing fragment isolation. However, all the remaining response variables did not respond to any other landscape variables in any spatial scale considered. Such contrasting responses of the abundances of eusocial vs. solitary species are related to the inherent life-history traits of each group. Important attributes in this context are different requirements on food resources, population features, and flight abilities. Species-specific dispersal abilities may be the main determinants of the nested patterns found for eusocial species at 1500 m. Considering these results, we suggest that different bee groups are considered separately in further landscape analyses, especially in other Brazilian biomes, for a better understanding of landscape effects on these organisms.

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

Similar content being viewed by others

References

  • Aizen MA, Sabatino M, Tylianakis JM (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 335:1486–1489

    Article  CAS  PubMed  Google Scholar 

  • Almeida-Neto M, Frensel DMB, Ulrich W (2012) Rethinking the relationship between nestedness and beta diversity: a comment on Baselga (2010). Glob Ecol Biogeogr 21:772–777

    Article  Google Scholar 

  • Araújo ED, Costa M, Chaud-Netto J, Fowler HG (2004) Body size and flight distance in stingless bees (Hymenoptera: Meliponini): inference of flight range and possible ecological implications. Rev Bras Biol 64:563–568

    Google Scholar 

  • Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143

    Article  Google Scholar 

  • Baselga A (2012) The relationship between species replacement, dissimilarity derived from nestedness, and nestedness. Glob Ecol Biogeogr 21:1223–1232

    Article  Google Scholar 

  • Baselga A, Orme D, Villeger S (2013) betapart: partitioning beta diversity into turnover and nestedness components. R package version 1.2. http://CRAN.R-project.org/package=betapart

  • Batalha MA, Mantovani W (2000) Reproductive phenological patterns of cerrado plant species at the Pé-de-Gigante Reserve (Santa Rita do Passa Quatro, SP, Brazil): a comparison between the herbaceous and woody floras. Rev Bras Biol 60:129–145

    Article  CAS  PubMed  Google Scholar 

  • Batalha MA, Martins FR (2004) Reproductive phenology of the cerrado plant community in Emas National Park (Central Brazil). Aust J Bot 52:149

    Article  Google Scholar 

  • Biesmeijer JC, Roberts SPM, Reemer M et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    Article  CAS  PubMed  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R, 1st edn. Springer, New York

    Book  Google Scholar 

  • Boscolo D, Metzger JP (2009) Is bird incidence in Atlantic forest fragments influenced by landscape patterns at multiple scales? Landsc Ecol 24:907–918

    Article  Google Scholar 

  • Brandão CRF, Silva RR, Feitosa RM (2011) Cerrado ground-dwelling ants (Hymenoptera: Formicidae) as indicators of edge effects. Zoologia 28:379–387

    Article  Google Scholar 

  • Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615

    Article  CAS  PubMed  Google Scholar 

  • Cameron SA, Lozier JD, Strange JP et al (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci U S A 108:662–667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kansas Entomol Soc 60:145–147

    Google Scholar 

  • Carvalho FMV, De Marco P Jr, Ferreira LG (2009) The Cerrado into-pieces: habitat fragmentation as a function of landscape use in the savannas of central Brazil. Biol Conserv 142:1392–1403

    Article  Google Scholar 

  • Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Article  Google Scholar 

  • Chust G, Pretus JL, Ducrot D et al (2003) Response of soil fauna to landscape heterogeneity: determining optimal scales for biodiversity modeling. Conserv Biol 17:1712–1723

    Article  Google Scholar 

  • Chust G, Pretus JL, Ducrot D, Ventura D (2004) Scale dependency of insect assemblages in response to landscape pattern. Landsc Ecol 19:41–57

    Article  Google Scholar 

  • Chust G, Pérez-Haase A, Chave J, Pretus JL (2006) Floristic patterns and plant traits of Mediterranean communities in fragmented habitats. J Biogeogr 33:1235–1245

    Article  Google Scholar 

  • Coddington JA, Griswold CE, Dávila DS et al (1991) Designing and testing sampling protocols to estimate biodiversity in tropical ecosystems. In: Dudley EC (ed) Critical issues in biodiversity. Dioscorides Press, Portland, p 17pp

    Google Scholar 

  • Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci 345:101–118

    Article  CAS  PubMed  Google Scholar 

  • Cozzi G, Müller CB, Krauss J (2007) How do local habitat management and landscape structure at different spatial scales affect fritillary butterfly distribution on fragmented wetlands? Landsc Ecol 23:269–283

    Article  Google Scholar 

  • Da Mata RA, Tidon R (2013) The relative roles of habitat heterogeneity and disturbance in drosophilid assemblages (Diptera, Drosophilidae) in the Cerrado. Insect Conserv Divers 6:663–670

    Article  Google Scholar 

  • Davies KF, Margules CR, Lawrence JF (2004) A synergistic effect puts rare, specialized species at greater risk of extinction. Ecology 85:265–271

    Article  Google Scholar 

  • R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing

  • Durães R, Martins WP, Vaz-de-Mello FZ (2005) Dung beetle (Coleoptera: Scarabaeidae) assemblages across a natural forest-Cerrado ecotone in Minas Gerais, Brazil. Neotrop Entomol 721–731

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Fahrig L, Baudry J, Brotons L et al (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112

    Article  PubMed  Google Scholar 

  • Faria LRR, Silveira FA (2011) The orchid bee fauna (Hymenoptera, Apidae) of a core area of the Cerrado, Brazil: the role of riparian forests as corridors for forest-associated bees. Biota Neotrop 11:87–94

    Article  Google Scholar 

  • Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280

    Article  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Winfree R et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 1608:1608–1611

    Article  Google Scholar 

  • Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71:757–764

    Article  Google Scholar 

  • Ghazoul J (2005) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol Evol 20:367–373

    Article  PubMed  Google Scholar 

  • Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596

    Article  PubMed  Google Scholar 

  • Heltshe JF, Forrester NE (1983) Estimating species richness using the jackknife procedure. Biometrics 39:1–11

    Article  CAS  PubMed  Google Scholar 

  • Henle K, Davies KF, Kleyer M et al (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251

    Article  Google Scholar 

  • Hill JK, Gray MA, Khen CV et al (2011) Ecological impacts of tropical forest fragmentation: how consistent are patterns in species richness and nestedness? Philos Trans R Soc Lond B Biol Sci 366:3265–3276. doi:10.1098/rstb.2011.0050

    Article  PubMed  PubMed Central  Google Scholar 

  • Hortal J, Roura-Pascual N, Sanders NJ, Rahbek C (2010) Understanding (insect) species distributions across spatial scales. Ecography 33:51–53

    Article  Google Scholar 

  • IBGE (2004) Mapa de biomas do Brasil. Escala 1:5.000.000. In: http://mapas.ibge.gov.br/biomas2/viewer.htm. Accessed on 11/09/2013

  • Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landsc Ecol 27:929–941

    Article  Google Scholar 

  • Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205

    Article  CAS  PubMed  Google Scholar 

  • Kadmon R (1995) Nested species subsets and geographic isolation: a case study. Ecology 76:458–465

    Article  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualism: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Kevan PG, Phillips TP (2001) The economic impacts of pollinator declines: an approach to assessing the consequences. Ecol Soc 5:Art. 8

    Google Scholar 

  • Klein AM, Vaissière BE, Cane JH et al (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274:303–313

    Article  Google Scholar 

  • Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19:707–713

    Article  Google Scholar 

  • Klink CA, Moreira AG (2002) Past and current human occupation, and land use. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 69–88

    Google Scholar 

  • Kuhn-Neto B, Contrera FAL, Castro MS, Nieh JC (2009) Long distance foraging and recruitment by a stingless bee, Melipona mandacaia. Apidologie 40:472–480

    Article  Google Scholar 

  • Kupfer JA, Malanson GP, Franklin SB (2006) Not seeing the ocean for the islands: the mediating influence of matrix-based processes on forest fragmentation effects. Glob Ecol Biogeogr 15:8–20

    Article  Google Scholar 

  • Le Féon V, Burel F, Chifflet R et al (2013) Solitary bee abundance and species richness in dynamic agricultural landscapes. Agric Ecosyst Environ 166:94–101

    Article  Google Scholar 

  • Lebuhn G, Droege S, Connor EF et al (2013) Detecting insect pollinator declines on regional and global scales. Conserv Biol 27:113–120

    Article  PubMed  Google Scholar 

  • Legendre P, Anderson M (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24

    Article  Google Scholar 

  • MacArthur RH, Levins R (1964) Competition, habitat selection, and character displacement in a patchy environment. Proc Natl Acad Sci U S A 51:1207–1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGarigal K, Marks BJ (1995) FRAGSTATS: spatial pattern analysis program for quantifying landscape structure

  • McKinney ML (1997) Extinction vulnerability and selection: combining ecological and paleontological views. Annu Rev Ecol Syst 28:495–516

    Article  Google Scholar 

  • Metzger JP (2000) Tree functional group richness and landscape structure in a Brazilian tropical fragmented landscape. Ecol Appl 10:1147–1161

    Article  Google Scholar 

  • Michener CD (2007) The bees of the world, 2nd edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Müller A, Diener S, Schnyder S et al (2006) Quantitative pollen requirements of solitary bees: implications for bee conservation and the evolution of bee–flower relationships. Biol Conserv 130:604–615

    Article  Google Scholar 

  • Murphy HT, Lovett-Doust J (2004) Context and connectivity in plant metapopulations and landscape mosaics: does the matrix matter? Oikos 105:3–14

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R et al (2013) vegan: community ecology package. R package version 2.0-9. http://CRAN.R-project.org/package=vegan

  • Pasquet RS, Peltier A, Hufford MB et al (2008) Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proc Natl Acad Sci U S A 105:13456–13461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinheiro F, Diniz IR, Coelho D, Bandeira MPS (2002) Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecol 27:132–136

    Article  Google Scholar 

  • Pivello VR, Carvalho VMC, Lopes PF et al (1999) Abundance and distribution of native and alien grasses in a “Cerrado” (Brazilian savanna) biological reserve. Biotropica 31:71–82

    Google Scholar 

  • Ricketts TH (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158:87–99

    Article  CAS  PubMed  Google Scholar 

  • Ricketts TH, Regetz J, Steffan-Dewenter I et al (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515

    Article  PubMed  Google Scholar 

  • Roubik DW (2001) Ups and downs in pollinator abundance peaks populations: when is there a decline? Conserv Ecol 5:article 2

    Article  Google Scholar 

  • Sano EE, Rosa R, Brito JLS, Ferreira LG (2008) Mapeamento semidetalhado do uso da terra do Bioma Cerrado. Pesq Agrop Brasileira 43:153–156

    Article  Google Scholar 

  • Schmidt MH, Thies C, Nentwig W, Tscharntke T (2007) Contrasting responses of arable spiders to the landscape matrix at different spatial scales. J Biogeogr 35:157–166

    Google Scholar 

  • Sheffield CS, Pindar A, Packer L, Kevan PG (2013) The potential of cleptoparasitic bees as indicator taxa for assessing bee communities

  • Silva DP, De Marco PJ (2014) No evidence of habitat loss affecting the orchid bees Eulaema nigrita Lepeletier and Eufriesea auriceps Friese (Apidae: Euglossini) in the Brazilian Cerrado Savanna. Neotrop Entomol 43:509–518

    Article  CAS  PubMed  Google Scholar 

  • Silveira FA, Campos MJO (1995) A melissofauna de Corumbataí (SP) e Paraopeba (MG) e uma análise da biogeografia das abelhas do Cerrado Brasileiro (Hymenoptera, Apoidea). Rev Bras Entomol 39:371–401

    Google Scholar 

  • Silveira FA, Cure JR (1993) High-altitude bee fauna of southeastern Brazil: implications for biogeographic patterns (Hymenoptera: Apoidea). Stud Neotropical Fauna Environ 28:47–55

    Article  Google Scholar 

  • Silveira FA, Melo GAR, Almeida EAB (2002) Abelhas brasileiras: sistemática e identificação, 1st edn. Edição do Autor, Belo Horizonte

    Google Scholar 

  • Steffan-Dewenter I, Munzenberg U, Burguer C et al (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432

    Article  Google Scholar 

  • Taki H, Kevan PG, Ascher JS (2007) Landscape effects of forest loss in a pollination system. Landsc Ecol 22:1575–1587

    Article  Google Scholar 

  • von Frisch K (1967) The dance language and orientation of bees, 1st edn. Harvard University Press, Cambridge

    Google Scholar 

  • Westphal C, Bommarco R, Carré G et al (2008) Measuring bee diversity in different European habitats and biogeographical regions. Ecol Monogr 78:653–671

    Article  Google Scholar 

  • Wikelski M, Moxley J, Eaton-Mordas A et al (2010) Large-range movements of Neotropical orchid bees observed via radio telemetry. PLoS One 5:e10738

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams NM, Minckley RL, Silveira FA (2001) Variation in native bee faunas and its implications for detecting community changes. Conserv Ecol 5:article 7

    Article  Google Scholar 

  • Williams NM, Crone EE, Roulston TH et al (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies, 1st edn. Belknap Press

  • Winfree R, Aguilar R, Vázquez DP et al (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076

    Article  PubMed  Google Scholar 

  • Wright DH, Patterson BD, Mikkelson GM et al (1998) A comparative analysis of nested subset patterns of species composition. Oecologia 113:1–20

    Article  Google Scholar 

  • Zapala MA, Schork NJ (2006) Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc Natl Acad Sci U S A 103:19430–19435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Pearson Prentice Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We would like to thank A. Bispo, F. M. V. Carvalho, and M.C. Almeida for discussions on the sampling design and for the help with the methodological issues involving landscape classification procedures and FRAGSTATS use. We are grateful to G.A.R. Melo, A. Aguiar, D. Parizotto, K. Ramos, L. Santos, R. Gonçalves, F. F. Oliveira, and A. Nemésio for bees’ identification and review of the bees’ life-history traits. Finally, we also thank P. Mendes, A. R. Rech, and an anonymous reviewer for valuable comments on previous versions of this text. DPS and PDMJ received financial support obtained from CNPq (477639/2010-0), Fundação “O Boticário” de Proteção à Natureza (0880/2010-2), and Whitley Wildlife Conservation Trust. The authors also would like to thank D. P. Silva Júnior, M. C. Almeida, and F. M. V. Carvalho who help in the field campaigns. DPS and DSN received scholarships from CNPq (147204/2010-0) and Coordenação de Aperfeiçoamento de Pessoal do Nível Superior – CAPES, respectively.

Author information

Authors and Affiliations

  1. Depto de Ciências Biológicas, Instituto Federal Goiano, Rodovia Geraldo Silva Nascimento, KM 2,5, Zona Rural, Urutaí, GO, Brasil, CEP 75790-000

    D P Silva

  2. Programa de Pós-Graduação em Ecologia e Evolução – Instituto de Ciências Biológicas – Campus II, Univ Federal de Goiás, Goiânia, GO, Brasil

    D S Nogueira

  3. Theory, Metapopulation, and Landscape Ecology Lab Depto de Ecologia Instituto de Ciências Biológicas – Campus II, Univ Federal de Goiás, Goiânia, GO, Brasil

    P De Marco Jr

Authors
  1. D P Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D S Nogueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P De Marco Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D P Silva.

Additional information

Edited by Wesley AC Godoy – ESALQ/USP

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 776 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silva, D.P., Nogueira, D.S. & De Marco, P. Contrasting Patterns in Solitary and Eusocial Bees While Responding to Landscape Features in the Brazilian Cerrado: a Multiscaled Perspective. Neotrop Entomol 46, 264–274 (2017). https://doi.org/10.1007/s13744-016-0461-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-016-0461-3

Keywords

Search

Navigation