Abstract
We aimed to evaluate the influence of climate and seasonality on the wild bee community from forest patches of an anthropic matrix located in a transition area between two biodiversity hotspots in southeastern Brazil using complementary sampling methods. The bees were sampled for all seasons of the year, using pan traps and sweep nets. We analyzed the bee community in terms of dominance, diversity, and equitability, to construct a description of the bee community in relation to its seasonal distribution. We studied the relationships between climatic variables, sampling methods, and seasonality for both individuals and species using generalized linear models. We collected a total of 805 individuals (non-Apis) belonging to 46 genera and 117 species. Although the sampling methods differed in terms of numbers of collected individuals, the methods were complementary regarding the species collected. Significant differences were observed in relation to the number of individuals and species across the seasons. The sampling method, precipitation, and temperature were the primary parameters identified as statistically significant in the bee survey. Autumn demonstrated the highest bee diversity, with a lower dominance and higher equitability compared to other seasons. Understanding how pollinators respond to different human-modified landscapes under various seasonal conditions in highly anthropic scenarios would improve conservation strategies for these pollinators in forest patches of an anthropic matrix.
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References
Abou-Shaara HF, Owayss AA, Ibrahim YY, Basuny NK (2017) A review of impacts of temperature and relative humidity on various activities of honey bees. Insect Soc 64:455–463. https://doi.org/10.1007/s00040-017-0573-8
Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918. https://doi.org/10.1016/j.cub.2009.03.071
Aleixo KP, Menezes C, Imperatriz Fonseca VL, da Silva CI (2016) Seasonal availability of floral resources and ambient temperature shape stingless bee foraging behavior (Scaptotrigona aff. depilis). Apidologie 48:117–127. https://doi.org/10.1007/s13592-016-0456-4
Arena MVN, Martines MR, da Silva TN, Destéfani FC, Mascotti JCS, Silva-Zacarin ECM, Toppa RH (2018a) Multiple-scale approach for evaluating the occupation of stingless bees in Atlantic Forest patches. For Ecol Manag 430:509–516. https://doi.org/10.1016/j.foreco.2018.08.038
Arena MVN, Destéfani FC, da Silva TN, Mascotti JCS, Silva-Zacarin ECM, Toppa RH (2018b) Challenges to the conservation of stingless bees in Atlantic Forest patches: old approaches, new applications. J Insect Conserv 22:627–633. https://doi.org/10.1007/s10841-018-0090-8
Bartón K (2016) MuMIn: Multi-Model Inference. R packages version 1.15.6. https://cran.rproject.org/web/packages/MuMIn/MuMIn.pdf
Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ (2011) Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS One 6:e23459. https://doi.org/10.1371/journal.pone.0023459
Boscolo D, Tokumoto PM, Ferreira PA, Ribeiro JW, dos Santos JS (2017) Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels. Perspect Ecol Conserv 15:18–24. https://doi.org/10.1016/j.pecon.2017.03.002
Brown MJ, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416. https://doi.org/10.1051/apido/2009019
Cane JH, Minckley RL, Kervin LJ, Roulston TH, Williams NM (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol Appl 16:632–644. https://doi.org/10.1890/1051-0761(2006)016[0632:CRWADB]2.0.CO;2
Cariveau DP, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci 10:104–109. https://doi.org/10.1016/j.cois.2015.05.004
Carper AL, Adler LS, Warren PS, Irwin RE (2014) Effects of suburbanization on forest bee communities. Environ Entomol 43:253–262. https://doi.org/10.1603/EN13078
Coelho S, Cardoso-Leite E, Castello ACD (2016) Floristic and successional characterization as a support for conservation and management of PNMCBIO, Sorocaba/SP. Ciênc Florestal 26:331–344. https://doi.org/10.5902/1980509821125
Cordeiro G, Boff S, Alves-dos-Santos I (2019) Trap-nesting bees communities from protected areas of Atlantic Forest, southeastern Brazil. Sociobiology 66:306–315. https://doi.org/10.13102/sociobiology.v66i2.3448
Corrêa LS, Cardoso-Leite E, Castello ACD, Coelho S, Kortz AR, Villela FNJ, Koch I (2014) Structure, floristic composition and successional characterization of fragments of Semideciduous seasonal Forest in Southeast Brazil. Rev Árvore 38:799–780. https://doi.org/10.1590/S0100-67622014000500004
Cristiano MP, Simões TG, Lopes DM, Pompolo SG (2014) Cytogenetics of Melitoma segmentaria (Fabricius, 1804) (Hymenoptera, Apidae) reveals differences in the characteristics of heterochromatin in bees. Comp Cytogenet 8:223–231. https://doi.org/10.3897/compcytogen.v8i3.7510
Dasgupta S, Mamingi N, Meisner C (2001) Pesticide use in Brazil in the era of agroindustrialization and globalization. Environ Dev Econ 6:459–482. https://doi.org/10.1017/s1355770x01000262
de Mattos IM, Souza J, Soares AEE (2018) Analysis of the effects of climate variables on Apis mellifera pollen foraging performance. Arq Bras Med Veterinária e Zootec 70:1301–1308. https://doi.org/10.1590/1678-4162-9373
de Mello K, Petri L, Cardoso-Leite EC, Toppa RH (2014) Cenários ambientais para o ordenamento territorial de áreas de preservação permanente no município de Sorocaba, SP. Rev Árvore 38:309–317. https://doi.org/10.1590/S0100-67622014000200011
de Mello K, Toppa RH, Cardoso-Leite EC (2016) Priority areas for forest conservation in an urban landscape at the transition between Atlantic Forest and Cerrado. Cerne 22:277–288. https://doi.org/10.1590/01047760201622032172
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Ann Rev Entom Stanford 52:81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, Suchail S, Brunet J-L, Alaux C (2013) Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS One 8:1–13. https://doi.org/10.1371/journal.pone.0072016
Fabian Y, Sandau N, Bruggisser OT, Aebi A, Kehrli P, Rohr RP, Naisbit RE, Bersier L-F (2013) The importance of landscape and spatial structure for hymenopteran-based food webs in an agro-ecosystem. J Anim Ecol 82:1203–1214. https://doi.org/10.1111/1365-2656.12103
Ferreira PA, Boscolo D, Carvalheiro LG, Biesmeijer JC, Rocha PLB, Viana BF (2015) Responses of bees to habitat loss in fragmented landscapes of Brazilian Atlantic rainforest. Landsc Ecol 30:2067–2078. https://doi.org/10.1007/s10980-015-0231-3
Fortel L, Henry M, Guilbaud L, Guirao AL, Kuhlmann M, Mouret H, Rollin O, Vaissière BE (2014) Decreasing abundance, increasing diversity and changing structure of the wild bee community (Hymenoptera: Anthophila) along an urbanization gradient. PLoS One 9:e104679. https://doi.org/10.1371/journal.pone.0104679
Françoso RD, Haidar RF, Machado RB (2016) Tree species of South America central savanna: endemism, marginal areas and the relationship with other biomes. Acta Bot Bras 30:78–86. https://doi.org/10.1590/0102-33062015abb0244
Gaglianone MC, Rocha HHS, Benevides CR, Junqueira CN, Augusto SC (2010) Importância de Centridini (Apidae) na polinização de plantas de interesse agrícola: o maracujá-doce (Passiflora alata curtis) como estudo de caso na região sudeste do Brasil. Oecologia Australis 14:152–164. https://doi.org/10.4257/oeco.2010.1401.08
Geslin B, Le Féon V, Folschweiller M, Flacher F, Carmignac D, Motard E, Perret S, Dajoz I (2016) The proportion of impervious surfaces at the landscape scale structures wild bee assemblages in a densely populated region. Ecol Evol 6:6599–6615. https://doi.org/10.1002/ece3.2374
Goulson D, Nicholls E (2016) The canary in the coalmine; bee declines as an indicator of environmental health. Sci Prog 99:312–326. https://doi.org/10.3184/003685016X14685000479908
Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. https://doi.org/10.1126/science.1255957
Hamblin AL, Youngsteadt E, Frank SD (2018) Wild bee abundance declines with urban warming, regardless of floral density. Urban Ecosyst 21:419–428. https://doi.org/10.1007/s11252-018-0731-4
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 9 pp. http://palaeo-electronica.org/2001_1/past/issue1_01.htm
Hatfield RG, LeBuhn G (2007) Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane meadows. Biol Conserv 139:150–158. https://doi.org/10.1016/j.biocon.2007.06.019
Hilário SD, Ribeiro MF, Imperatriz-Fonseca VL (2007) Impacto da precipitação pluviométrica sobre a atividade de vôo de Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Biota Neotrop 7:135–143 Available at http://www.biotaneotropica.org.br/v7n3/pt/abstract?article+bn02307032007
Hopfenmüller S, Steffan-Dewenter I, Holzschuh A (2014) Trait-specific responses of wild bee communities to landscape composition, configuration and local factors. PLoS One 9:1–10. https://doi.org/10.1371/journal.pone.0104439
IBGE, Instituto Brasileiro de Geografia e Estatítica (2002) Climatologia. https://www.ibge.gov.br/geociencias-novoportal/informacoes-ambientais/climatologia.html. Accessed 21 November 2018
INMET, Instituto Nacional de Meteorologia (2018) Banco de Dados Meteorológicos para Ensino e Pesquisa. http://wwwinmetgovbr/projetos/rede/pesquisa/ Accessed 23 October 2018
Kortz AR, Coelho S, Castello ACD, Cardoso-Leite E, Corrêa LS, Koch I (2014) Wood vegetation in Atlantic rain forest remnants in Sorocaba (São Paulo, Brazil). Check List 10:344–354. https://doi.org/10.15560/10.2.344
Kovach WL (2007) MVSP - a MultiVariate statistical package for windows, ver. 3.1. Kovach computing services, Pentraeth, Wales, UK
LeBuhn G, Roulston T, Tepedino V, Griswold T, Minckley R, Droege S, Cane J, Parker F, Buchmann S, Williams N, Kremen C, Messenger O (2003) A standardized method for monitoring bee populations–the bee inventory (BI) plot. http://online.sfsu.edu/beeplot/pdfs/Bee%20Plot%202003.pdf. Accessed 16 July 2014
Liebsch D, Marques MCM, Goldenberg R (2008) How long does the Atlantic rain Forest take to recover after a disturbance? Changes in species composition and ecological features during secondary succession. Biol Conserv 141:1717–1725. https://doi.org/10.1016/j.biocon.2008.04.013
Magura T, Lövei GL, Tóthmérész B (2017) Edge responses are different in edges under natural versus anthropogenic influence: a meta-analysis using ground beetles. Ecol Evol 7:1009–1017. https://doi.org/10.1002/ece3.2722
Maia-Silva C, Imperatriz-Fonseca VL, Silva CI, Hrncir M (2014) Environmental windows for foraging activity in stingless bees, Melipona subnitida Ducke and Melipona quadrifasciata Lepeletier (Hymenoptera: Apidae: Meliponini). Sociobiology 61:378–385. https://doi.org/10.13102/sociobiology.v61i4.378-385
Mamede-Filho GF, Ramos MA, Oliveira AG (1991) Contribuição à biologia da Melitoma segmentaria (Anthophoridae). Rev Bras Zool, Curitiba 7:217–221. https://doi.org/10.1590/S0101-81751990000300003
Martins RP, Guerra STM, Barbeitos MS (2001) Variability in egg to adult development time in the bee Ptilothrix plumata and its parasitoids. Ecol Entom 26:609–616. https://doi.org/10.1046/j.1365-2311.2001.00353.x
Martins AC, Silva DP, de Marco JP, Melo GAR (2014) Species conservation under future climate change: the case of Bombus bellicosus, a potentially threatened south American bumblebee species. J Insect Conserv 19:33–43. https://doi.org/10.1007/s10841-014-9740-7
Matias DMS, Leventon J, Rau AL, Borgemeister C, von Wehrden H (2017) A review of ecosystem service benefits from wild bees across social contexts. Ambio 46:456–467. https://doi.org/10.1007/s13280-016-0844-z
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005
Medeiros RLS, Aguiar WM, Aguiar CML, Borges IGM (2017) The orchid bee communities in different phytophysiognomies in the Atlantic forest: from lowland to montane rainforests. Sociobiology 64:182–190. https://doi.org/10.13102/sociobiology.v64i2.1348
Michener CD (2007) The bees of the world. JHU Press, Baltimore
Moeller DA, Geber MA, Eckhart VM, Tiffin P (2012) Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology 93:1036–1048. https://doi.org/10.1890/11-1462.1
Moral RA, Hinde J, Demétrio CGB (2017) Half-normal plots and overdispersed models in R: the hnp package. J Stat Softw 81:1–23
Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62. https://doi.org/10.1016/S0169-5347(00)88977-6
Nemésio A, Silveira FA (2007) Diversity and distribution of orchid bees (Hymenoptera: Apidae) with a revised checklist of species. Neotrop Entomol 36:874–888. https://doi.org/10.1590/S1519-566X2007000600008
Ogilvie JE, Griffin SR, Gezon ZJ, Inouye BD, Underwood N, Inouye DW, Irwin RE (2017) Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology. Ecol Lett 20:1507–1515. https://doi.org/10.1111/ele.12854
Oliveira R, Schlindwein C (2010) Experimental demonstration of alternative mating tactics of male Ptilothrix fructifera (Hymenoptera, Apidae). Anim Behav 80:241–247. https://doi.org/10.1016/j.anbehav.2010.04.024
Polatto LP, Chaud-Netto J, Alves-Junior VV (2014) Influence of abiotic factors and floral resource availability on daily foraging activity of bees. J Insect Behav 27:593–612. https://doi.org/10.1007/s10905-014-9452-6
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/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, Austria. URL https://www.R-project.org
Ries L, Sisk TD (2004) A predictive model of edge effects. Ecology 85:2917–2926. https://doi.org/10.1890/03-8021
Ripley B, Venables B, Bates D, Hornik K, Gebhardt A, Firth D (2014) Support functions and datasets for Venables and Ripley’s MASS. R package version 7:3–35
Sakagami SF, Laroca S, Moure JS (1967) Wild bee biocenotics in São José dos Pinhais (PR), South Brazil. Preliminary report. J Fac Sci Hokkaido Univ 16:253–291 http://hdl.handle.net/2115/27447
Sárospataki M, Báldi A, Batáry P, Józan Z, Erdős S, Rédei T (2009) Factors affecting the structure of bee assemblages in extensively and intensively grazed grasslands in Hungary. Commun Ecol 10:182–188. https://doi.org/10.1556/ComEc.10.2009.2.7
Schlindwein C (1998) Frequent oligolecty characterizing a diverse bee plant community in a xerophytic bushland of subtropical Brazil. Stud Neot Fau Env Lisse 33:46–59. https://doi.org/10.1076/snfe.33.1.46.2168
Schlindwein C, Martins CF (2000) Competition between the oligolectic bee Ptilothrix plumata (Anthophoridae) and the flower closing beetle Pristimerus calcaratus (Curculionidae) for floral resources of Pavonia cancellata (Malvaceae). Plant Syst Evol 224(3–4):183–194. https://doi.org/10.1007/BF00986342
Schlindwein C, Pick RA, Martins CF (2012) Coleta de alimento por uma abelha solitária (Ptilothrix plumata) da Caatinga. In: Semana dos Polinizadores, 3. Palestras e resumos. Petrolina: Embrapa Semiárido. p. 173–184
Settele J, Bishop J, Potts SG (2016) Climate change impacts on pollination. Nat Plants 2:1–3. https://doi.org/10.1038/nplants.2016.92
Silveira FA, Melo GAR, Almeida EAB (2002) Abelhas brasileiras: sistemática e identificação. Fundação Araucária, Belo Horizonte
Slaa EJ (2006) Population dynamics of a stingless bee community in the seasonal dry lowlands of Costa Rica. Insect Soc 53:70–79. https://doi.org/10.1007/s00040-005-0837-6
Stone GN, Gilbert F, Willmer P, Potts S, Semida F, Zalat S (1999) Windows of opportunity and the temporal structuring of foraging activity in a desert solitary bee. Ecol Entomol 24:208–221. https://doi.org/10.1046/j.1365-2311.1999.00181.x
Viana BF, Boscolo D, Neto EM, Lopes LE, Lopes AV, Ferreira PA, Pigozzo CM, Primo LM (2012) How well do we understand landscape effects on pollinators and pollination services. J Pollinat Ecol 7:31–41
Vilhena PDS, Rocha L, Garófalo CA (2017) Male orchid bees (Hymenoptera: Apidae: Euglossini) in canopy and understory of Amazon Várzea floodplain Forest. I. Microclimatic, seasonal and faunal aspects. Sociobiology 64:191. https://doi.org/10.13102/sociobiology.v64i2.1232
Vrdoljak S, Samways M (2012) Optimising colored pan traps to survey flower visiting insects. J Insect Conserv 16:345–354. https://doi.org/10.1007/s10841-011-9420-9
Winfree R (2010) The conservation and restoration of wild bees. Ann N Y Acad Sci 1195:169–197. https://doi.org/10.1111/j.1749-6632.2010.05449.x
Winfree R, Griswold T, Kremen C (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv Biol 21:213–223. https://doi.org/10.1111/j.1523-1739.2006.00574.x
Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees responses to anthropogenic disturbance. Ecology 90:2068–2076. https://doi.org/10.1890/08-1245
Wojcik VA, Frankie GW, Thorp RW, Hernandez JL (2008) Seasonality in bees and their floral resource plants at a constructed urban bee habitat in Berkeley, California. J Kansas Entomol Soc 81:15–28. https://doi.org/10.2317/JKES-701.17.1
Yuan F, Bauer ME (2007) Comparison of impervious surface area and normalized difference vegetation index as indicators of surface urban heat island effects in Landsat imagery. Remote Sens Environ 106:375–386. https://doi.org/10.1016/j.rse.2006.09.003
Acknowledgments
We thank the Center of Environmental Education of SEMA (the Secretary of the Environment of the city of Sorocaba) for the permission to study bee fauna in Biquinha Park. We thank Mr. Pedro for the permission to study bee fauna at the São Pedro Farm. We are very grateful to Rafael Alexandre Costa Ferreira for his help in designing the pan traps used in this study. We also deeply thank Dr. Eduardo Andrade Botelho de Almeida, professor at the Bee Laboratory (USP - FFCLRP, Ribeirão Preto, Brazil) and Dr. Fernando Amaral da Silveira, professor at the Laboratory for Bee Systematics and Ecology (UFMG, Belo Horizonte, Brazil) for assisting us with the taxonomic identification of the bees. We thank the blind reviewers for all the suggestions that guided us to improve the manuscript. The authors thank the support of FAPESP (2017/21097-3).
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The first author thanks CAPES for the funding during her academic study in the Postgraduate Program in Biotechnology and Environmental Monitoring (PPGBMA) at UFSCar-Sorocaba.
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de Assis, J.C., Toppa, R.H., Martines, M.R. et al. The influence of climate and seasonality on bee communities: a complementary method for bee sampling in forest patches of an anthropic matrix. Int J Trop Insect Sci 41, 711–723 (2021). https://doi.org/10.1007/s42690-020-00261-1
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DOI: https://doi.org/10.1007/s42690-020-00261-1