Patterns of diversity in a metacommunity of bees and wasps of relictual mountainous forest fragments

  • Lucas Neves PerilloEmail author
  • Newton Pimentel de Ulhôa Barbosa
  • Ricardo R. C. Solar
  • Frederico de Siqueira Neves


Naturally fragmented landscapes provide a suitable opportunity for investigating species dynamics under the sole influence of habitat fragmentation. Various approaches have used landscape attributes (e.g., patch size and connectivity) to explain patterns of species diversity and composition. We evaluated the influence that patch and landscape attributes have on bee and wasp (Hymenoptera: Aculeata) diversity (species richness and abundance) using a natural forest archipelago located in a campo rupestre (rupestrian grassland) matrix. We also assessed the effects of season on species composition (temporal β-diversity). Our analysis found higher richness and abundance of bees and wasps in the summer. There was a significant change in species composition between seasons (species replacement accounts for 88% of β-diversity), with winter communities not representing subsets of summer communities. Evaluation of the relationships between bee and wasp diversity and landscape attributes (e.g., patch size and isolation, distance between patches and continuous forest distance), only found a significant relationship for temporal β-diversity, which increases with distance from continuous forest. We propose that forest islands can be considered transient environments for many species, and so this naturally fragmented metacommunity depends on continuous forest propagules and its temporal dynamics to sustain diversity among forest islands.


Spatio-temporal patterns Atlantic forest Community structure Landscape structure Fragmentation Campo rupestre 



We would like to thank the following students from the Insect Ecology Lab for assistance with field work: Luiz Eduardo Macedo Reis, Flávio Siqueira de Castro, Daniela Melo, Luiz Fernando Ferreira, Geanne Pereira, Humberto Brant and Heron Hilário, and we highlight the invaluable help of Caio Silveira Marques and Thaís Silva Tavares. We extend our gratitude to G. Wilson Fernandes for providing climatic data; Reserva Vellozia and GSG for logistical support; José Eustáquio dos Santos Júnior and Rogério Lopes for specimen identification; and Francisco Carvalho Diniz and Pedro Giovâni da Silva for text revision. Dr. Marcel Coelho provided very important advice regarding the project and provided insightful comments regarding the text. This study was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Conselho Nacional de Desenvolvimento Científico e Tecnológico (Long-Term Ecological Research PELD-CRSC-17) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10841_2019_194_MOESM1_ESM.docx (207 kb)
Supplementary material 1 (DOCX 207 kb)


  1. Abrahamczyk S, Kluge J, Gareca Y et al (2011) The influence of climatic seasonality on the diversity of different tropical pollinator groups. PLoS ONE 6:e27115. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alves RJV, Silva NG, Oliveira JA, Medeiros D (2014) Circumscribing campo rupestre: megadiverse Brazilian rocky montane savanas. Braz J Biol 74:355–362. CrossRefPubMedGoogle Scholar
  3. Banks-Leite C, Ewers RM, Metzger JP (2012) Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes. Ecology 93:2560–2569. CrossRefPubMedGoogle Scholar
  4. Barbosa O, Marquet PA, Bacigalupe LD et al (2010) Interactions among patch area, forest structure and water fluxes in a fog-inundated forest ecosystem in semi-arid Chile. Funct Ecol 24:909–917. CrossRefGoogle Scholar
  5. Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. CrossRefGoogle Scholar
  6. Baselga A (2012) The relationship between species replacement, dissimilarity derived from nestedness, and nestedness. Glob Ecol Biogeogr 21:1223–1232. CrossRefGoogle Scholar
  7. Basset Y, Cizek L, Cuenoud P et al (2012) Arthropod diversity in a tropical forest. Science 338:1481–1484. CrossRefPubMedGoogle Scholar
  8. Benedick S, Hill JK, Mustaffa N et al (2006) Impacts of rain forest fragmentation on butterflies in northern Borneo: species richness, turnover and the value of small fragments. J Appl Ecol 43:967–977. CrossRefGoogle Scholar
  9. Biswas SR, Wagner HH (2012) Landscape contrast: a solution to hidden assumptions in the metacommunity concept? Landsc Ecol 27:621–631. CrossRefGoogle Scholar
  10. Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Breiman L (2001) Random forests. Mach Learn 45:5–32. CrossRefGoogle Scholar
  12. Brotons L, Mönkkönen M, Martin JL (2003) Are fragments islands? Landscape context and density-area relationships in boreal forest birds. Am Nat 162:343–357. CrossRefPubMedGoogle Scholar
  13. Carvalho Guimarães CD, Viana JPR, Cornelissen T (2014) A meta-analysis of the effects of fragmentation on herbivorous insects. Environ Entomol 43:537–545. CrossRefPubMedGoogle Scholar
  14. Coddington JA, Agnarsson I, Miller JA et al (2009) Undersampling bias: the null hypothesis for singleton species in tropical arthropod surveys. J Anim Ecol 78:573–584. CrossRefPubMedGoogle Scholar
  15. Coelho MS, Fernandes GW, Pacheco P et al (2016) Archipelago of montane forests surrounded by rupestrian grasslands: new insights and perspectives. In: Fernandes GW (ed) Ecology and conservation of mountaintop grasslands in Brazil. Springer, Cham, pp 129–156CrossRefGoogle Scholar
  16. Coelho MS, Carlos PP, Pinto VD et al (2018a) Connection between tree functional traits and environmental parameters in an archipelago of montane forests surrounded by rupestrian grasslands. Flora Morphol Distrib Funct Ecol Plants 238:51–59. CrossRefGoogle Scholar
  17. Coelho MS, Neves FS, Perillo LN et al (2018b) Forest archipelagos: a natural model of metacommunity under the threat of fire. Flora Morphol Distrib Funct Ecol Plants 238:244–249. CrossRefGoogle Scholar
  18. Cook WM, Lane KT, Foster BL, Holt RD (2002) Island theory, matrix effects and species richness patterns in habitat fragments. Ecol Lett 5:619–623. CrossRefGoogle Scholar
  19. Cook WM, Anderson RM, Schweiger EW (2004) Is the matrix really inhospitable? Vole runway distribution in an experimentally fragmented landscape. Oikos 104:5–14. CrossRefGoogle Scholar
  20. Corrêa MM, Fernandes GW, Leal IR (2006) Diversidade de formigas epigéicas (Hymenoptera: Formicidae) em capões do pantanal sul matogrossense: relações entre riqueza de espécies e complexidade estrutural da área. Neotrop Entomol 35:724–730. CrossRefPubMedGoogle Scholar
  21. Crawley MJ (2013) The R book, 2nd edn. Wiley, ChichesterGoogle Scholar
  22. Cuissi RG, Lasmar CJ, Moretti TS et al (2015) Ant community in natural fragments of the Brazilian wetland: species–area relation and isolation. J Insect Conserv 19:531–537. CrossRefGoogle Scholar
  23. da Silva PG, Nunes CA, Ferreira LF et al (2019) Patch and landscape effects on forest-dependent dung beetles are masked by matrix-tolerant dung beetles in a mountaintop rainforest archipelago. Sci Total Environ 651:1321–1331. CrossRefPubMedGoogle Scholar
  24. Dall’Oglio OT, Ribeiro RC, De Souza RF et al (2016) Can the understory affect the hymenoptera parasitoids in a eucalyptus plantation? PLoS ONE 11:e0151165. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Derraik JGB, Early JW, Closs GP, Dickinson KJM (2010) Morphospecies and taxonomic species comparison for hymenoptera. J Insect Sci 10:1–7. CrossRefGoogle Scholar
  26. Dormann CF, Elith J, Bacher S et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:027–046. CrossRefGoogle Scholar
  27. Driscoll DA (2005) Is the matrix a sea? Habitat specificity in a naturally fragmented landscape. Ecol Entomol 30:8–16. CrossRefGoogle Scholar
  28. Driscoll DA (2008) The frequency of metapopulations, metacommunities and nestedness in a fragmented landscape. Oikos 117:297–309. CrossRefGoogle Scholar
  29. Fernández F, Sharkey MJ (2006) Introducción a los hymenoptera de la región neotropical. Editora Guadalupe Ltda, BogotáGoogle Scholar
  30. Frazer GW, Canham CD, Lertzman KP (1999) Gap light analyzer (GLA), version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. ©1999 Simon Fraser Univ. Burn. Br. Columbia, Inst. Ecosyst. Stud. Millbrook, New YorkGoogle Scholar
  31. Giulietti AM, Pirani JR, Harley RM (1997) Espinhaço range region—Eastern Brazil. In: Davis SD, Heywood VH, Herrera-MacBryde O et al (eds) Centres of plant diversity: a guide and strategy for their conservation -, vol 3. The Americas. WWF/IUCN Publications Unit, Cambridge, pp 397–404Google Scholar
  32. Haddad NM, Holt RD, Fletcher RJ et al (2017) Connecting models, data, and concepts to understand fragmentation’s ecosystem-wide effects. Ecography 40:1–8. CrossRefGoogle Scholar
  33. Haila Y (2002) A conceptual genealogy of fragmentation research: from island biogeography to landscape ecology. Ecol Appl 12:321–334Google Scholar
  34. Hopper SD, Silveira FAO, Fiedler PL (2016) Biodiversity hotspots and Ocbil theory. Plant Soil 403:167–216. CrossRefGoogle Scholar
  35. Inclán DJ, Cerretti P, Marini L (2014) Interactive effects of area and connectivity on the diversity of tachinid parasitoids in highly fragmented landscapes. Landsc Ecol 29:879–889. CrossRefGoogle Scholar
  36. Jamoneau A, Chabrerie O, Closset-Kopp D, Decocq G (2012) Fragmentation alters beta-diversity patterns of habitat specialists within forest metacommunities. Ecography 35:124–133. CrossRefGoogle Scholar
  37. Julião GR, Amaral MEC, Fernandes GW, Oliveira EG (2004) Edge effect and species–area relationships in the gall-forming insect fauna of natural forest patches in the Brazilian Pantanal. Biodivers Conserv 13:2055–2066. CrossRefGoogle Scholar
  38. Leibold MA, Holyoak M, Mouquet N et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. CrossRefGoogle Scholar
  39. Levins R (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull Entomol Soc Am 15:237–240. CrossRefGoogle Scholar
  40. Lion MB, Garda AA, Santana DJ, Fonseca CR (2016) The conservation value of small fragments for atlantic forest reptiles. Biotropica 48:265–275. CrossRefGoogle Scholar
  41. MacArthur RH, Wilson OE (1967) The theory of island biogeography. Princeton University Press, PrincetonGoogle Scholar
  42. Macedo-Reis LE, Quesada M, de Siqueira Neves F (2019) Forest cover drives insect guild diversity at different landscape scales in tropical dry forests. For Ecol Manage 443:36–42. CrossRefGoogle Scholar
  43. Magrach A, Laurance WF, Larrinaga AR, Santamaria L (2014) Meta-analysis of the effects of forest fragmentation on interspecific interactions. Conserv Biol 28:1342–1348. CrossRefPubMedGoogle Scholar
  44. McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous mapsGoogle Scholar
  45. Mello-Silva R, Santos DYAC, Salatino MLF et al (2011) Five vicarious genera from Gondwana: the Velloziaceae as shown by molecules and morphology. Ann Bot 108:87–102. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Mendenhall CD, Karp DS, Meyer CFJ et al (2014) Predicting biodiversity change and averting collapse in agricultural landscapes. Nature 509:213–217. CrossRefPubMedGoogle Scholar
  47. Misiewicz TM, Kraichak E, Rasmussen C (2014) Distance and habitat drive fine scale stingless bee (Hymenoptera: Apidae) community turnover across naturally heterogeneous forests in the Western Amazon. Sociobiology 61:407–414. CrossRefGoogle Scholar
  48. Mota GS, Luz GR, Mota NM et al (2018) Changes in species composition, vegetation structure, and life forms along an altitudinal gradient of rupestrian grasslands in south-eastern Brazil. Flora Morphol Distrib Funct Ecol Plants 238:32–42. CrossRefGoogle Scholar
  49. Nassar JM, Rodríguez JP, Sánchez-Azofeifa A et al (2008) Manual of methods: human, ecological and biophysical dimensions of tropical dry forests. Gráficas Lauki C.A, CaracasGoogle Scholar
  50. Neves FS, Oliveira VHF, Espírito-Santo MM et al (2010) Successional and seasonal changes in a community of dung beetles (Coleoptera: Scarabaeinae) in a Brazilian tropical dry forest. Braz J Nat Conserv 8:160–164. CrossRefGoogle Scholar
  51. Nogueira AA, Pinto-da-Rocha R (2016) The effects of habitat size and quality on the orb-weaving spider guild (Arachnida: Araneae) in an atlantic forest fragmented landscape. J Arachnol 44:36–45. CrossRefGoogle Scholar
  52. Novais SMA, Nunes CA, Santos NB et al (2016) Effects of a possible pollinator crisis on food crop production in Brazil. PLoS ONE 11:1–12. CrossRefGoogle Scholar
  53. Nunes CA, Braga RF, Figueira JEC et al (2016) Dung beetles along a tropical altitudinal gradient: environmental filtering on taxonomic and functional diversity. PLoS ONE 11:e0157442. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Öckinger E, Lindborg R, Sjödin NE, Bommarco R (2012) Landscape matrix modifies richness of plants and insects in grassland fragments. Ecography 35:259–267. CrossRefGoogle Scholar
  55. Oles A, Pau G, Smith M, et al (2012) EBImage: 4.10.1., community ecology package. R package versionGoogle Scholar
  56. Oliver I, Beattie AJ (1996) Invertebrate morphospecies as surrogates for species: a case study. Conserv Biol 10:99–109. CrossRefGoogle Scholar
  57. Oliver I, Dorrough J, Doherty H, Andrew NR (2016) Additive and synergistic effects of land cover, land use and climate on insect biodiversity. Landsc Ecol 31:2415–2431. CrossRefGoogle Scholar
  58. Osborne JL, Clark SJ, Morris RJ et al (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. J Appl Ecol 36:519–533. CrossRefGoogle Scholar
  59. Patiño J, Whittaker RJ, Borges PAV et al (2017) A roadmap for island biology: 50 fundamental questions after 50 years of the theory of island biogeography. J Biogeogr 44:963–983. CrossRefGoogle Scholar
  60. Pereira GCN, Coelho MS, Beirão MV et al (2017) Diversity of fruit-feeding butterflies in a mountain archipelago of rainforest. PLoS ONE 12:e0180007. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Perillo LN, Neves FS, Antonini Y, Martins RP (2017) Compositional changes in bee and wasp communities along neotropical mountain altitudinal gradient. PLoS ONE 12:e0182054. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Prugh LR, Hodges KE, Sinclair ARE, Brashares JS (2008) Effect of habitat area and isolation on fragmented animal populations. Proc Natl Acad Sci USA 105:20770–20775. CrossRefPubMedGoogle Scholar
  63. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  64. Rocha NMWB, Carstensen DW, Fernandes GW et al (2016) Phenology patterns across a rupestrian grassland altitudinal gradient. In: Fernandes GW (ed) Ecology and conservation of mountaintop grasslands in Brazil. Springer, Cham, pp 275–289CrossRefGoogle Scholar
  65. Rossetti MR, Tscharntke T, Aguilar R, Batáry P (2017) Responses of insect herbivores and herbivory to habitat fragmentation: a hierarchical meta-analysis. Ecol Lett 20:264–272. CrossRefPubMedGoogle Scholar
  66. Silva NAP, Frizzas MR, Oliveira CM (2011) Seasonality in insect abundance in the “Cerrado” of Goiás State, Brazil. Rev Bras Entomol 55:79–87. CrossRefGoogle Scholar
  67. Silveira FA, Melo GAR, Almeida EAB (2002) Abelhas Brasileiras: sistemática e identificação. Belo HorizonteGoogle Scholar
  68. Silveira FAO, Negreiros D, Barbosa NPU et al (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403:129–152. CrossRefGoogle Scholar
  69. Soares SA, Suarez YR, Fernandes WD et al (2013) Temporal variation in the composition of ant assemblages (Hymenoptera, Formicidae) on trees in the Pantanal floodplain, Mato Grosso do Sul, Brazil. Rev Bras Entomol 57:84–90. CrossRefGoogle Scholar
  70. Solar RRC, Barlow J, Ferreira J et al (2015) How pervasive is biotic homogenization in human-modified tropical forest landscapes? Ecol Lett 18:1108–1118. CrossRefPubMedGoogle Scholar
  71. Suni SS, Bronstein JL, Brosi BJ (2014) Spatio-temporal genetic structure of a tropical bee species suggests high dispersal over a fragmented landscape. Biotropica 46:202–209. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Thompson PL, Rayfield B, Gonzalez A (2017) Loss of habitat and connectivity erodes species diversity, ecosystem functioning, and stability in metacommunity networks. Ecography 40:98–108. CrossRefGoogle Scholar
  73. Tscharntke T, Steffan-Dewenter I, Kruess A, Thies C (2002) Characteristics of insect populations on habitat fragments: a mini review. Ecol Res 17:229–239. CrossRefGoogle Scholar
  74. Tscharntke T, Tylianakis JM, Rand TA et al (2012) Landscape moderation of biodiversity patterns and processes: eight hypotheses. Biol Rev 87:661–685. CrossRefPubMedGoogle Scholar
  75. Tuomisto H (2010) A diversity of beta diversities: Straightening up a concept gone awry. Part 1. Defining beta diversity as a function of alpha and gamma diversity. Ecography 33:2–22. CrossRefGoogle Scholar
  76. Tylianakis JM, Klein AM, Tscharntke T (2005) Spatiotemporal variation in the effects of a tropical habitat gradient on Hymenoptera diversity. Ecology 86:3296–3302. CrossRefGoogle Scholar
  77. Van Nouhuys S, Hanski I (2002) Colonization rates and distances of a host butterfly and two specific parasitoids in a fragmented landscape. J Anim Ecol 71:639–650. CrossRefGoogle Scholar
  78. Vieira L, Lopes FS, Fernandes WD, Raizer J (2008) Comunidade de carabidae (Coleoptera) em manchas florestais no pantanal, Mato Grosso do Sul, Brasil. Iheringia Série Zool 98:317–324. CrossRefGoogle Scholar
  79. Walters BB, Stiles EW (1996) Effect of canopy gaps and flower patch size on pollinator visitation of Impatiens capensis. Bull Torrey Bot Club 123:184–188. CrossRefGoogle Scholar
  80. Watling JI, Donnelly MA (2006) Fragments as islands: a synthesis of faunal responses to habitat patchiness. Conserv Biol 20:1016–1025. CrossRefPubMedGoogle Scholar
  81. Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251. CrossRefGoogle Scholar
  82. Wolda H (1988) Insect seasonality: why? Annu Rev Ecol Syst 19:1–18. CrossRefGoogle Scholar
  83. Yekwayo I, Pryke JS, Roets F, Samways MJ (2016) Surrounding vegetation matters for arthropods of small, natural patches of indigenous forest. Insect Conserv Divers 9:224–235. CrossRefGoogle Scholar
  84. Zehm A, Nobis M, Schwabe A (2003) Multiparameter analysis of vertical vegetation structure based on digital image processing. Flora Morphol Distrib Funct Ecol Plants 198:142–160. CrossRefGoogle Scholar
  85. Zurbuchen A, Landert L, Klaiber J et al (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143:669–676. CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratório de Ecologia de Insetos, Instituto de Ciências BiológicasUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Departamento de Genética, Ecologia e Evolução, Instituto de Ciências BiológicasUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  3. 3.Bocaina Biologia da ConservaçãoBelo HorizonteBrazil

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