Skip to main content

Advertisement

Log in

Orchid bees respond to landscape composition differently depending on the multiscale approach

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

Multiscale approaches are essential for understanding ecological processes and detecting the scale of effect. However, nested multiscale approaches retain the effect of the landscape attributes from the smaller spatial scales into the larger ones. Thus, decoupling the nested scales can reveal detailed ecological responses to landscape context, but this multiscale approach is poorly explored.

Objectives

We evaluated the scale of effect of the forest cover (%) and landscape heterogeneity on Euglossini bee communities combining coupled and decoupled multiscale approaches.

Methods

The Euglossini males were sampled in forest patches from 15 landscapes within the Atlantic Forest, southeast Brazil. For simplicity, we defined that the coupled approaches represented the local scales and decoupled the regional scales. We decoupled the scales by cutting out the smaller scales inserted into larger ones. We estimated the relationship of the bee community attributes with forest cover (%) and landscape heterogeneity in local and regional scales using Generalized Linear Models.

Results

We found a trend of positive effects of landscape heterogeneity on species richness for decoupled regional scales. Forest cover and landscape heterogeneity on coupled local scales positively affected the Euglossini species abundance. The scale of effect for Euglossini species abundance was on coupled local scales.

Conclusions

Combining coupled and decoupled multiscale approaches was essential to determine the scale of effect of the landscape composition on bee communities. Therefore, it is crucial to measure the influence of the landscape context on biodiversity. Maintaining landscapes with larger forest cover and spatial heterogeneity is important for bee requirements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Additional data is available in supplementary material.

Code availability

Not applicable.

References

  • Ackerman JD (1989) Geographic and seasonal variation in fragrance choices and preferences of male Euglossine bees. Biotropica 21(4):340–347

    Google Scholar 

  • Aguiar WM, Sofia SH, Melo GA, Gaglianone MC (2015) Changes in orchid bee communities across forest-agroecosystem boundaries in Brazilian Atlantic forest landscapes. Environ Entomol 44(6):1465–1471

    PubMed  Google Scholar 

  • Allen TFH, Hoekstra TW (1991) Role of heterogeneity in scaling of ecological systems under analysis. In: Kolasa J, Pickett STA (eds) Ecological heterogeneity. Springer, New York, pp 47–68

    Google Scholar 

  • Allen TFH, Starr TB (1982) Hierarchy perspective for ecological complexity. University of Chicago Press, Chicago

    Google Scholar 

  • Allen L, Reeve R, Nousek-McGregor A, Villacampa J, MacLeod R (2019) Are orchid bees useful indicators of the impacts of human disturbance? Ecol Indic 103:745–755

    Google Scholar 

  • Amiot C, Santos CC, Arvor D, Bellón B, Fritz H, Harmange C, Holland JD, Melo I, Metzger JP, Renaud PC, Roque FO, Souza FL, Pays O (2021) The scale of effect depends on operational definition of forest cover evidence from terrestrial mammals of the Brazilian savanna. Landsc Ecol 36(4):973–987

    Google Scholar 

  • Arroyo-Rodríguez V, Rojas C, Saldaña-Vázquez RA, Stoner KE (2016) Landscape composition is more important than landscape configuration for phyllostomid bat assemblages in a fragmented biodiversity hotspot. Biol Conserv 198:84–92

    Google Scholar 

  • Barton K (2020) MuMIn: multi-model inference. R package version 1.43.17. Available at https://CRAN.R-project.org/package=MuMIn

  • Basu P, Parui AK, Chatterjee S, Dutta A, Chakraborty P, Roberts S, Smith B (2016) Scale dependent drivers of wild bee diversity in tropical heterogeneous agricultural landscapes. Ecol Evol 6(19):6983–6992

    PubMed  PubMed Central  Google Scholar 

  • Ben Bolker and R Development Core Team (2020) bbmle: tools for general maximum likelihood estimation. R package version 1.0.23.1. Available at https://CRAN.R-project.org/package=bbmle

  • Boscolo D, Metzger JP (2009) Is bird incidence in Atlantic forest fragments influenced by landscape patterns at multiple scales? Landsc Ecol 24(7):907–918

    Google Scholar 

  • Boscolo D, Tokumoto PM, Ferreira PA, Ribeiro JW, Santos JS (2017) Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels. Perspect Ecol Conserv 15(1):18–24

    Google Scholar 

  • Brennan JM, Bender DJ, Contreras TA, Fahrig L (2002) Focal patch landscape studies for wildlife management: optimizing sampling effort across scales. In: Liu J, Taylor WW (eds) Integrating landscape ecology into natural resource management. Cambridge University Press, Cambridge, pp 68–91

    Google Scholar 

  • Brosi BJ (2009) The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biol Conserv 142(2):414–423

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65(1):23–35

    Google Scholar 

  • Cândido MEMB, Morato EF, Storck-Tonon D, Miranda PN, Vieira LJS (2018) Effects of fragments and landscape characteristics on the orchid bee richness (Apidae: Euglossini) in an urban matrix, southwestern Amazonia. J Insect Conserv 22(3–4):475–486

    Google Scholar 

  • Carneiro LS, Aguiar WM, Priante CF, Ribeiro MC, Frantine-Silva W, Gaglianone MC (2021) The interplay between thematic resolution, forest cover, and heterogeneity for explaining Euglossini bees community in an agricultural landscape. Front Ecol Evol. https://doi.org/10.3389/fevo.2021.628319

    Article  Google Scholar 

  • Collevatti RG, Santos JS, Rosa FF, Amaral TS, Chaves LJ, Ribeiro MC (2020) Multi-scale landscape influences on genetic diversity and adaptive traits in a neotropical Savanna tree. Front Genet 11:259

    PubMed  PubMed Central  Google Scholar 

  • Cushman SA, Landguth EL (2010) Scale dependent inference in landscape genetics. Landsc Ecol 25(6):967–979

    Google Scholar 

  • Dressler RL (1982) Biology of the orchid bees (Euglossini). Annu Rev Ecol Evol Syst 13(1):373–394

    Google Scholar 

  • Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol S 48(1):1–23

    Google Scholar 

  • Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller RJ, Sirami C, Siriwardena GM, Martin JL (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14(2):101–112

    PubMed  Google Scholar 

  • Ferreira-Caliman MJ, Rocha-Filho LC, Freiria GA, Garófalo CA (2018) Floral sources used by the orchid bee Euglossa cordata (Linnaeus, 1758) (Apidae: Euglossini) in an urban area of south-eastern Brazil. Grana 57(6):471–480

    Google Scholar 

  • Franceschinelli EV, Elias MAS, Bergamini LL, Silva-Neto CM, Sujii ER (2017) Influence of landscape context on the abundance of native bee pollinators in tomato crops in Central Brazil. J Insect Conserv 21(4):715–726

    Google Scholar 

  • Frantine-Silva W, Augusto SC, Tosta THA, Pacheco AS, Kotelok-Diniz T, Apolinário CS, Sofia SH (2021) Genetic diversity and population structure of orchid bees from the Brazilian savanna. J Apic Res 60(3):385–395

    Google Scholar 

  • Freiria GA, Ruim JB, Souza RF, Sofia SH (2011) Population structure and genetic diversity of the orchid bee Eufriesea violacea (Hymenoptera, Apidae, Euglossini) from Atlantic Forest remnants in southern and southeastern Brazil. Apidologie 43(4):392–402

    Google Scholar 

  • Fundação SOS Mata Atlântica INPE (2021) Atlas dos remanescentes florestais da Mata Atlântica: período 2019/2020, relatório técnico. Fundação SOS Mata Atlântica, São Paulo

    Google Scholar 

  • Galán-Acedo C, Arroyo-Rodríguez V, Cudney-Valenzuela SJ, Fahrig L (2019) A global assessment of primate responses to landscape structure. Biol Rev 94(5):1605–1618

    PubMed  Google Scholar 

  • Garófalo CA (1985) Social structure of Euglossa cordata nests (Hymenoptera: Apidae: Euglossini). Entomol Gen 11(1–2):77–83

    Google Scholar 

  • Gestich CC, Arroyo-Rodríguez V, Ribeiro MC, Cunha RG, Setz EZF (2018) Unraveling the scales of effect of landscape structure on primate species richness and density of titi monkeys (Callicebus nigrifrons). Ecol Res 34(1):150–159

    Google Scholar 

  • Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM, Damschen EI et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1(2):e1500052

    PubMed  PubMed Central  Google Scholar 

  • Herrmann HL, Babbitt KJ, Baber MJ, Congalton RG (2005) Effects of landscape characteristics on amphibian distribution in a forest-dominated landscape. Biol Conserv 123(2):139–149

    Google Scholar 

  • Hesselbarth MHK, Sciaini M, With KA, Wiegand K, Nowosad J (2019) landscapemetrics: an open-source R tool to calculate landscape metrics. Ecography 42(10):1648–1657

    Google Scholar 

  • Holland JD, Bert DG, Fahrig L (2004) Determining the spatial scale of species’ response to habitat. Bioscience 54(3):227–233

    Google Scholar 

  • Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landsc Ecol 27(7):929–941

    Google Scholar 

  • Jackson ND, Fahrig L (2014) Landscape context affects genetic diversity at a much larger spatial extent than population abundance. Ecology 95(4):871–881

    PubMed  Google Scholar 

  • Jackson HB, Fahrig L (2015) Are ecologists conducting research at the optimal scale? Glob Ecol Biogeogr 24(1):52–63

    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(1):8–20

    Google Scholar 

  • Levin SA (1992) The problem of pattern and scale in Ecology: The Robert H. MacArthur Award lecture. Ecology 73(6):1943–1967

    Google Scholar 

  • Lyra-Jorge MC, Ribeiro MC, Ciocheti G, Tambosi LR, Pivello VR (2010) Influence of multi-scale landscape structure on the occurrence of carnivorous mammals in a human-modified savanna, Brazil. Eur J Wildl Res 56(3):359–368

    Google Scholar 

  • Machado T, Viana BF, Silva CI, Boscolo D (2020) How landscape composition affects pollen collection by stingless bees? Landsc Ecol 35(3):747–759

    Google Scholar 

  • Martin AE (2018) The spatial scale of a species’ response to the landscape context depends on which biological response you measure. Curr Landsc Ecol Rep 3(1):23–33

    Google Scholar 

  • McGarigal K (2015) FRAGSTATS help. University of Massachusetts, Amherst

    Google Scholar 

  • Miguet P, Jackson HB, Jackson ND, Martin AE, Fahrig L (2016) What determines the spatial extent of landscape effects on species? Landsc Ecol 31(6):1177–1194

    Google Scholar 

  • Milne BT (1991) Heterogeneity as a multiscale characteristic of landscapes. In: Kolasa J, Pickett STA (eds) Ecological heterogeneity. Springer, New York, pp 69–84

    Google Scholar 

  • Miranda EA, Nascimento Lima I, Oi CA, López-Uribe MM, Del Lama MA, Freitas BM, Silva CI (2021) Overlap of ecological niche breadth of Euglossa cordata and Eulaema nigrita (Hymenoptera, Apidae, Euglossini) accessed by pollen loads and species distribution modeling. Neotrop Entomol 50(2):197–207

    PubMed  Google Scholar 

  • Montagnana PC, Alves RS, Garófalo CA, Ribeiro MC (2021) Landscape heterogeneity and forest cover shape cavity-nesting hymenopteran communities in a multi-scale perspective. Basic Appl Ecol 56:239–249

    Google Scholar 

  • Morante-Filho JC, Arroyo-Rodríguez V, Faria D (2016) Patterns and predictors of β-diversity in the fragmented Brazilian Atlantic forest: a multiscale analysis of forest specialist and generalist birds. J Anim Ecol 85(1):240–250

    PubMed  Google Scholar 

  • Nagy-Reis MB, Estevo CA, Setz EZF, Ribeiro MC, Chiarello AG, Nichols JD (2017) Relative importance of anthropogenic landscape characteristics for Neotropical frugivores at multiple scales. Anim Conserv 20(6):520–531

    Google Scholar 

  • Newman EA, Kennedy MC, Falk DA, McKenzie D (2019) Scaling and complexity in landscape ecology. Front Ecol Evol. https://doi.org/10.3389/fevo.2019.00293

    Article  Google Scholar 

  • O’Neill RV, Hunsaker CT, Timmins SP, Jackson BL, Jones KB, Riitters KH, Wickham JD (1996) Scale problems in reporting landscape pattern at the regional scale. Landsc Ecol 11(3):169–180

    Google Scholar 

  • Opedal ØH, Martins AA, Marjakangas EL (2020) A database and synthesis of euglossine bee assemblages collected at fragrance baits. Apidologie 51:519–530

    Google Scholar 

  • Pokorny T, Loose D, Dyker G, Quezada-Euán JJG, Eltz T (2015) Dispersal ability of male orchid bees and direct evidence for long-range flights. Apidologie 46(2):224–237

    Google Scholar 

  • Püttker T, Crouzeilles R, Almeida-Gomes M, Schmoeller M, Maurenza D, Alves-Pinto H, Pardini R, Vieira MV, Banks-Leite C, FonsecaCR MJP, Accacio GM et al (2020) Indirect effects of habitat loss via habitat fragmentation: a cross-taxa analysis of forest-dependent species. Biol Conserv 241:108368

    Google Scholar 

  • Ramalho AV, Gaglianone MC, Oliveira ML (2009) Comunidades de abelhas Euglossina (Hymenoptera, Apidae) em fragmentos de Mata Atlântica no Sudoeste do Brasil. Rev Bras Entomol 53(1):95–101

    Google Scholar 

  • Ramalho M, Rosa JF, Dantas E, Silva M, Silva M, Monteiro D (2013) Spatial distribution of orchid bees in a rainforest/rubber agro-forest mosaic: habitat use or connectivity. Apidologie 44(4):385–403

    Google Scholar 

  • Rhodes JR, McAlpine CA, Zuur AF, Smith GM, Ieno EN (2009) GLMM applied on the spatial distribution of koalas in a fragmented landscape. In: Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (eds) Mixed effects models and extensions in ecology with R. Springer, Stanford, pp 469–492

    Google Scholar 

  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142(6):1141–1153

    Google Scholar 

  • Rocha-Filho LC, Krug C, Silva CI, Garófalo CA (2012) Floral resources used by Euglossini bees (Hymenoptera: Apidae) in coastal ecosystems of the Atlantic Forest. Psyche. https://doi.org/10.1155/2012/934951

    Article  Google Scholar 

  • Rosa JF, Ramalho M, Monteiro D, Silva MD (2015) Permeability of matrices of agricultural crops to Euglossina bees (Hymenoptera, Apidae) in the Atlantic Rain Forest. Apidologie 46(6):691–702

    Google Scholar 

  • Roubik DW, Hanson PE (2004) Orchids bees of tropical America: biology and field guide. INBio Press, Heredia

    Google Scholar 

  • Shukla A, Jain K (2019) Critical analysis of spatial-temporal morphological characteristic of urban landscape. Arab J Geosc. https://doi.org/10.1007/s12517-019-4270-y

    Article  Google Scholar 

  • Silva M, Hartling L, Opps SB (2005) Small mammals in agricultural landscapes of Prince Edward Island (Canada): effects of habitat characteristics at three different spatial scales. Biol Conserv 126(4):556–568

    Google Scholar 

  • Steffan-Dewenter I (2002) Landscape context affects trap-nesting bees, wasps, and their natural enemies. Ecol Entomol 27(5):631–637

    Google Scholar 

  • Storck-Tonon D, Peres CA (2017) Forest patch isolation drives local extinctions of Amazonian orchid bees in a 26 years old archipelago. Biol Conserv 214:270–277

    Google Scholar 

  • Stuber EF, Fontaine JJ (2019) How characteristic is the species characteristic selection scale? Glob Ecol Biogeogr 28(12):1839–1854

    Google Scholar 

  • Turner MG (1989) Landscape ecology: the effect of pattern on process. Annu Rev Ecol Evol Syst 20(1):171–197

    Google Scholar 

  • Turner MG, Gardner RH (2015) Landscape ecology in theory and practice. Springer, New York

    Google Scholar 

  • Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3(4):385

    Google Scholar 

  • Wikelski M, Moxley J, Eaton-Mordas A, López-Uribe MM, Holland R, Moskowitz D, Roubik DW, Kays R (2010) Large-range movements of neotropical orchid bees observed via radio telemetry. PLoS ONE 5(5):e10738

    PubMed  PubMed Central  Google Scholar 

  • Wu J (2004) Effects of changing scale on landscape pattern analysis: scaling relations. Landsc Ecol 19(2):125–138

    Google Scholar 

  • Wu J (2007) Scale and scaling: a cross-disciplinary perspective. In: Wu J, Hobbs RJ (eds) Key topics in landscape ecology. Cambridge University Press, Cambridge, pp 15–142

    Google Scholar 

  • Zucchi R, Sakagami SF, Camargo JM (1969) Biological observations on a neotropical parasocial bee, Eulaema nigrita, with a review on the biology of Euglossinae (Hymenoptera, Apidae): a comparative study. 北海道大學理學部紀要 17(2):271–380

    Google Scholar 

Download references

Acknowledgements

We are grateful to the Bee Ecology and Pollination Lab team (LCA-UENF) for their field help; the owners for authorizing sampling on their properties; Dr. Gabriel Augusto Rodrigues de Melo (UFPR) for taxonomic confirmation; Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis—IBAMA for the permission to collected biological material; Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq, Ministério da Ciência, Tecnologia, Inovações e Comunicações—MCTIC, IBAMA, Associação Brasileira de Estudo das Abelhas—A.B.E.L.H.A. for project financing (CNPq/MCTIC/IBAMA/A.B.E.L.H.A. 400614/2018-9), and the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro—FAPERJ for financial support.

Funding

We thank the CNPq/MCTIC/IBAMA/A.B.E.L.H.A. for financial support (project 400614/2018-9). LSC and CFP thank FAPERJ for the scholarship. LSC and WFS thank CAPES for the scholarship (processes 88887.339454/2019-00; 88882.314552/2019-01). MCG thanks CNPq (process 303894/2018-0) and FAPERJ (process 203.321/2017) for their financial support. MCR thanks FAPESP (processes 2013/50421-2; 2020/01779-5; 2021/08534-0; 2021/10195-0), CNPq (processes 312045/2013-1; 312292/2016-3; 442147/2020-1; 402765/2021-4; 313016/2021-6) and PROCAD/CAPES (project 88881.068425/2014-01) for their financial support.

Author information

Authors and Affiliations

Authors

Contributions

MCG, LSC, and WMA idealized the study design. MCR delimited the multiscale approaches. LSC, MCG, and MCR idealized the main hypotheses. LSC and MCR quantified the landscape metrics. LSC, MCR, and WFS analyzed the data. CFP and LSC did the spatial analysis. All authors contributed to the manuscript revision.

Corresponding author

Correspondence to Lázaro da Silva Carneiro.

Ethics declarations

Conflict of interest

Not applicable.

Ethical approval

The authorization for collect biological material was provided by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis-IBAMA (N° 71013-3).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 258 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva Carneiro, L., Ribeiro, M.C., Aguiar, W.M. et al. Orchid bees respond to landscape composition differently depending on the multiscale approach. Landsc Ecol 37, 1587–1601 (2022). https://doi.org/10.1007/s10980-022-01442-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-022-01442-8

Keywords

Navigation