Abstract
Context
In human-altered landscapes, native vegetation cover is essential for pollination maintenance. Heterogeneous land-uses may provide complementary resources for some pollinator species, contributing to the connectivity of landscapes and the maintenance of pollination.
Objectives
To investigate the effect of forest cover and non-forest landscape heterogeneity on pollination of native understory forest plant assemblages.
Methods
We quantified pollen deposited on understory native flowers in gradients of forest cover and heterogeneity of land-uses (Shannon–Wiener diversity index) in a central forest patch in 14 landscapes.
Results
Forest cover and the non-forest heterogeneity of land-uses interacted, favoring pollination in landscapes with high amount of forest and low heterogeneity, and in landscapes with low amount of forest and high heterogeneity. Forest promotes high-quality habitats and higher connectivity for pollinators, increasing pollination. Forest cover and non-forest landscape heterogeneity seemed to increase pollinator efficiency, since pollination increased regardless of pollinator diversity. In landscapes with a low amount of forest, high land-use heterogeneity may partially compensate for forest loss due to land-uses that offered complementary resources for the maintenance of pollinators and pollination.
Conclusions
We have seen that pollination is favored by forest cover and the interaction between native forest and other land-uses that can add complementary resources and landscape connectivity to pollinators. For management policies, priority should be on the maintenance and increase of native forest cover in the landscapes, followed by promoting heterogeneity of other favorable land-uses to pollinators.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980. https://doi.org/10.1111/j.1461-0248.2006.00927.x
Ahrné K, Bengtsson J, Elmqvist T (2009) Bumble Bees (Bombus spp) along a gradient of increasing urbanization. PLoS ONE 4:e5574. https://doi.org/10.1371/journal.pone.0005574
Aizen MA, Feinsinger P (1994a) Forest fragmentation, pollination, and plant reproduction in a chaco dry forest, Argentina. Ecology 75:330–351
Aizen MA, Feinsinger P (1994b) Habitat fragmentation, native insect pollinators, and feral honeybees in Argentine “Chaco Serrano.” Ecol Appl 4:378–392
Aizen MA, Ashworth L, Galetto L (2002) Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter? J Veg Sci 13:885–892. https://doi.org/10.1111/J.1654-1103.2002.Tb02118.X
Aizen MA, Sabatino M, Tylianakis JM (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science 80(335):1486–1489. https://doi.org/10.1126/science.1215320
Alonso C, Navarro-Fernández CM, Arceo-Gómez G, Meindl GA, Parra-Tabla V, Ashman T (2013) Among-species differences in pollen quality and quantity limitation: implications for endemics in biodiverse hotspots. Ann Bot 112(7):1461–1469. https://doi.org/10.1093/aob/mct213
Andersson GKS, Rundlöf M, Smith HG (2012) Organic farming improves pollination success in strawberries. PLoS ONE 7(2):e31599. https://doi.org/10.1371/journal.pone.0031599
Andersson GKS, Birkhofer K, Rundlöf M, Smith HG (2013) Landscape heterogeneity and farming practice alter the species composition and taxonomic breadth of pollinator communities. Basic Appl Ecol 14(7):540–546. https://doi.org/10.1016/j.baae.2013.08.003
Arceo-Gómez G, Abdala-Roberts L, Jankowiak A, Kohler C, Meindl GA, Navarro-Fernández CM, Parra-Tabla V, Ashman T, Alonso C (2016) Patterns of among- and within-species variation in heterospecific pollen receipt: the importance of ecological generalization. Am J Bot 103:396–407. https://doi.org/10.3732/ajb.1500155
Bawa KS (1990) Plant-pollinator interactions in tropical rain forests. Annu Rev Ecol Syst 21(1):399–422. https://doi.org/10.1146/annurev.es.21.110190.002151
Bjorkman T (1995) The effect of pollen load and pollen grain competition on fertilization success and progeny performance in Fagopyrum esculentum. Euphytica 83:47–52. https://doi.org/10.1007/BF01677860
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 15:18–24. https://doi.org/10.1016/j.pecon.2017.03.002
BRASIL LEI Nº 8.171, De 17 de Janeiro De 1991, provides for agricultural policy
Breitbach N, Tillmann S, Schleuning M, Grünewald C, Laube I, Steffan-Dewenter I, Böhning-Gaese K (2012) Influence of habitat complexity and landscape configuration on pollination and seed-dispersal interactions of wild cherry trees. Oecologia 168:425–437. https://doi.org/10.1007/s00442-011-2090-1
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400
Burnham KP, Anderson DR (1998) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Calviño-Cancela M, Rubido-Bará M, van Etten EJB (2012) Do eucalypt plantations provide habitat for native forest biodiversity? For Ecol Manage 270:153–162. https://doi.org/10.1016/j.foreco.2012.01.019
Cepagri (2017) Centro de pesquisas meteorológicas e climáticas aplicadas à agricultura. Clima dos municípios paulistas. https://www.cpa.unicamp.br/cepagri/previsao. Accessed 2 May 2020.
Chatterjee A, Chatterjee S, Smith B (2020) Predicted thresholds for natural vegetation cover to safeguard pollinator services in agricultural landscapes. Agr Ecosyst Environ 290:106785. https://doi.org/10.1016/j.agee.2019.106785
Consul PC, Famoye F (1992) Generalized poisson regression model. Commun Stat 21:89–109. https://doi.org/10.1080/03610929208830766
Cranmer L, Mccollin D, Ollerton J (2012) Landscape structure influences pollinator movements and directly affects plant reproductive success. Oikos 121:562–568. https://doi.org/10.1111/j.1600-0706.2011.19704.x
Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond B 267:1149–1152. https://doi.org/10.1098/rspb.2000.1121
DataGeo 2020. Infraestrutura de Dados Espaciais Ambientais do Estado de São Paulo. Accessed 25 February 2020
De Blois S, Domon G, Bouchard A (2002) Landscape issues in plant ecology. Ecography 25:244–256. https://doi.org/10.1034/j.1600-0587.2002.250212.x
Ebeling A, Klein A, Schumacher J, Weisser WW, Tscharntke T (2008) How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos 117:1808–1815. https://doi.org/10.1111/j.1600-0706.2008.16819.x
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller RJ, Sirami C, Siriwardena GM, Martin J-L (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112. https://doi.org/10.1111/j.1461-0248.2010.01559.x
Feinsinger P, Tiebout HM III, Young BE (1991) Do tropical bird-pollinated plants exhibit density-dependent interaction? Field experiments. Ecology 72:1953–1963. https://doi.org/10.2307/1941550
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
Ferreira PA, Boscolo D, Lopes LE, Carvalheiro LG, Biesmeijer JC, Rocha PLB, Viana BF (2020) Forest and connectivity loss simplify tropical pollination networks. Oecologia 192:577–590. https://doi.org/10.1007/s00442-019-04579-7
Geslin B, Gauzens B, Thébault E, Dajoz I (2013) Plant pollinator networks along a gradient of urbanisation. PLoS ONE 8(5):e63421. https://doi.org/10.1371/journal.pone.0063421
González-Varo JP, Vilà M (2017) Spillover of managed honeybees from mass-flowering crops into natural habitats. Biol Conserv 212:376–382. https://doi.org/10.1016/j.biocon.2017.06.018
Governo do Estado de São Paulo (2009) SIFESP, Sistema de Informações Florestais do Estado de São Paulo
Guiller C, Affre L, Albert CH et al (2016) How do field margins contribute to the functional connectivity of insect-pollinated plants? Landsc Ecol 31:1747–1761. https://doi.org/10.1007/s10980-016-0359-9
Hadley AS, Betts MG (2012) The effects of landscape fragmentation on pollination dynamics: absence of evidence not evidence of absence. Biol Rev 87:526–544. https://doi.org/10.1111/j.1469-185X.2011.00205.x
Hadley AS, Frey SJK, Robinson WD, Kress WJ, Betts MG (2014) Tropical forest fragmentation limits pollination of a keystone understory herb. Ecology 95:2202–2212. https://doi.org/10.1890/13-0929.1
Hagen M, Kraemer M (2010) Agricultural surroundings support flower-visitor networks in an Afrotropical rain forest. Biol Conserv 143:1654–1663. https://doi.org/10.1016/j.biocon.2010.03.036
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(8):e104439. https://doi.org/10.1371/journal.pone.0104439
Kaluza BF, Wallace H, Heard TA, Klein A, Leonhardt SD (2016) Urban gardens promote bee foraging over natural habitats and plantations. Ecol Evol 6:1304–1316. https://doi.org/10.1002/ece3.1941
Kammerer M, Biddinger D, Rajotte E, Mortensen D (2016) Local plant diversity across multiple habitats supports a diverse wild bee community in Pennsylvania apple orchards. Environ Entomol 45:32–38. https://doi.org/10.1093/ee/nvv147
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot
Kennedy CM, Lonsdorf E, Neel MC et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. https://doi.org/10.1111/ele.12082
Klein A, Cunnigham SA, Bos M, Steffan-Dewenter I (2008) Advances in pollination ecology from tropical plantation crops. Ecology 89(4):935–943. https://doi.org/10.1890/07-0088.1
Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816. https://doi.org/10.1073/pnas.262413599
Lázaro A, Alomar D (2019) Landscape heterogeneity increases the spatial stability of pollination services to almond trees through the stability of pollinator visits. Agric Ecosyst Environ 279:149–155. https://doi.org/10.1016/j.agee.2019.02.009
Lienert J (2004) Habitat fragmentation effects of fitness of plant populations—a review. J Nat Conserv 12:53–72. https://doi.org/10.1016/j.jnc.2003.07.002
Lindgren J, Lindborg R, Cousins SAO (2018) Local conditions in small habitats and surrounding landscape are important for pollination services, biological pest control and seed predation. Agric Ecosyst Environ 251:107–113. https://doi.org/10.1016/j.agee.2017.09.025
Locke H, Ellis EC, Venter O, Schuster R, Ma K, Shen X, Woodley S, Kingston N, Bhola N, Strassburg BBN, Paulsch A, Williams B, Watson JEM (2019) Three global conditions for biodiversity conservation and sustainable use: an implementation framework. Natl Sci Rev 6(6):1080–1082. https://doi.org/10.1093/nsr/nwz136
Lopes LE, Buzato S (2007) Variation in pollinator assemblages in a fragmented landscape and its effects on reproductive stages of a self-incompatible treelet, Psychotria suterella (Rubiaceae). Oecologia 154:305–314. https://doi.org/10.1007/s00442-007-0830-z
MacArthur RH, Wilson EO (2001) The theory of island biogeography. Princeton University Press, Princeton
Machado T, Viana BF, da Silva CI, Boscolo D (2020) How landscape composition affects pollen collection by stingless bees? Landsc Ecol 35:747–759. https://doi.org/10.1007/s10980-020-00977-y
Martin FM (1959) Staining and observing pollen tubes by means of fluorescence. Stain Technol 34:436–437
McGarigal K, Cushman SA, 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. Accessed http://www.umass.edu/landeco/research/fragstats/fragstats.html
Moreira EF, Boscolo D, Viana BF (2015) Spatial heterogeneity regulates plant—pollinator networks across multiple landscape scales. PLoS ONE 10(4):e0123628. https://doi.org/10.1371/journal.pone.0123628
Morellato LPC, Haddad CFB (2000) Introduction: the Brazilian Atlantic forest. Biotropica 32:786–792. https://doi.org/10.1111/j.1744-7429.2000.tb00618.x
Myers N, Mittermeier R, Mittermeier C, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Naeem S (2002) Ecosystem consequences of biodiversity loss: the evolution of a paradigm. Ecology 83:1537–1552. https://doi.org/10.1890/0012-9658(2002)083[1537:ECOBLT]2.0.CO;2
Nakamura S, Kudo G (2019) The influence of garden flowers on pollinator visits to forest flowers: comparison of bumblebee habitat use between urban and natural areas. Urban Ecosyst 22:1097–1112. https://doi.org/10.1007/s11252-019-00891-5
Nason JD, Hamrick JL (1997) Reproductive and genetic consequences of forest fragmentation: two case studies of neotropical canopy trees. J Hered 88:264–276. https://doi.org/10.1093/oxfordjournals.jhered.a023104
Nery LS, Takata JT, Camargo BB, Chaves AM, Ferreira PA, Boscolo D (2018) Bee diversity responses to forest and open areas in heterogeneous Atlantic forest. Sociobiology 65:686–695. https://doi.org/10.13102/sociobiology.v65i4.3472
Parra-Tabla V, Vargas CF, Magaña-Rueda S, Navarro J (2000) Female and male pollination success of Oncidium ascendens Lindey (Orchidaceae) in two contrasting habitat patches. Biol Cons 94:335–340. https://doi.org/10.1016/S0006-3207(99)00187-1
Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, Dicks LV, Garibaldi LA, Hill R, Settele J, Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229. https://doi.org/10.1038/nature20588
Rocha-Santos L, Benchimol M, Mayfield MM, Faria D, Pessoa MS, Talora DC, Mariano-Neto E, Cazetta E (2017) Functional decay in tree community within tropical fragmented landscapes: effects of landscape-scale forest cover. PLoS ONE 12:e0175545. https://doi.org/10.1371/journal.pone.0175545
San Martin-Gajardo I, Morellato LPC (2003) Fenologia de Rubiaceae do sub-bosque em floresta Atlântica no sudeste do Brasil. Rev Bras Bot 26:299–309. https://doi.org/10.1590/s0100-84042003000300003
São Paulo (2017) Governo do Estado, Secretaria Municipal de Meio Ambiente -Resolução SMA Nº 7 e SMA Nº 32 de 18 de janeiro de 2017
Saturni FT, Jaffé R, Metzger JP (2016) Landscape structure influences bee community and coffee pollination at different spatial scales. Agric Ecosyst Environ 235:1–12. https://doi.org/10.1016/j.agee.2016.10.008
Schüepp C, Herzog F, Entling MH (2013) Disentangling multiple drivers of pollination in a landscape-scale experiment. Proc R Soc B. https://doi.org/10.1098/rspb.2013.2667
Soares RGS, Ferreira PA, Lopes LE (2017) Can plant-pollinator network metrics indicate environmental quality? Ecol Indic 78:361–370. https://doi.org/10.1016/j.ecolind.2017.03.037
Souza T M (2019) Paisagens agrícolas funcionais: modelagem como ferramenta para a conservação de polinizadores e bem-estar social. Tese de Doutorado, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto. doi:https://doi.org/10.11606/T.59.2020.tde-13032020-102035
Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432. https://doi.org/10.1890/0012-9658(2002)083[1421:SDEOLC]2.0.CO;2
Taki H, Kevan PG (2007) Does habitat loss affect the communities of plants and insects equally in plant—pollinator interactions? Preliminary findings. Biodivers Conserv 16:3147–3161. https://doi.org/10.1007/s10531-007-9168-4
Taki H, Kevan PG, Ascher JS (2007) Landscape effects of forest loss in a pollination system. Landsc Ecol 22:1575–1587. https://doi.org/10.1007/s10980-007-9153-z
Whately M, Cunha P (2007) Cantareira 2006: um olhar sobre o maior manancial de água da região metropolitana de São Paulo. São Paulo, Instituto Socioambiental
Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends Plant Sci 7(6):270–277. https://doi.org/10.1016/s1360-1385(02)02258-6
Williams NM, Winfree R (2013) Local habitat characteristics but not landscape urbanization drive pollinator visitation and native plant pollination in forest remnants. Biol Conserv 160:10–18. https://doi.org/10.1016/j.biocon.2012.12.035
Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10:1105–1113. https://doi.org/10.1111/j.1461-0248.2007.01110.x
Woodcock BA, Bullock JM, McCracken M, Chapman RE, Ball SL, Edwards ME, Nowakowski M, Pywell RF (2016) Spill-over of pest control and pollination services into arable crops. Agric Ecosyst Environ 231:15–23. https://doi.org/10.1016/j.agee.2016.06.023
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
We are grateful to the Landscape Ecology and Analysis Pack (LEAP, USP—Ribeirão Preto, SP) for the team work during field sampling, to Milton C. Ribeiro and all the Spatial Ecology and Conservation Laboratory (LEEC, UNESP—Rio Claro, SP) team for land cover classification of our study region, to the farmers that kindly allowed us to conduct our study on their lands, and to Rodrigo S. Rodrigues, Daniele Monteiro, Cíntia Kameyama, Fabrício S. Meyer, Guilherme M. Antar, Luís C. Bernacci, Maria Alves, Matheus Nogueira, Nádia Roque, Rafael Trevisan, José R. Barosela and Milton Groppo who aided us with plant identifications. We also thank the Department of Physiological Sciences at the Federal University of São Carlos and Gustavo Marega Oda, Heloisa Sobreiro Selistre de Araújo, Marisa Narciso Fernandes from the Zoophysiology and Comparative Biochemistry Laboratory (LZBC) for their help with microscopes. To the entire TAPIRI-UFSCar team. To reviewers for careful reading and valuable contributions to growth for this study.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. PAF Postdoctoral Scholarship financed by the National Postdoctoral Program of the Coordination for the Improvement of Higher Education Personnel—PNPD-CAPES. RGSS master's grant financed by the Coordination for the Improvement of Higher Education Personnel—CAPES. Research funding (Project Plant-pollinator interaction networks in heterogeneous landscapes of Atlantic Forest—Ministry of Science, Technology and Innovations with the National Council for Scientific and Technological Development (MCTI / CNPq)/Universal 449740/2014-5). The São Paulo Research Foundation—FAPESP for funding the project New sampling methods and statistical tools for biodiversity research: integrating animal movement ecology with population and community ecology (process 2013/50421–2).
Author information
Authors and Affiliations
Contributions
All authors contributed to the conceptual elaboration of the project leading to the development of this study. RGSS and PAF performed data collection in the field. RGSS and ACR did the laboratory analysis. RGSS and LEL made the landscapes and statistical analysis. PAF and DB were responsible for financing this study. All authors contributed to the preparation and revision of this text.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest or competing interest with the publication of this study.
Consent to participate
All authors declare their consent to participate in this study.
Consent for publication
All authors declare their consent to the publication of this study.
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.
Rights and permissions
About this article
Cite this article
Soares, R.G.S., Ferreira, P.A., Boscolo, D. et al. Forest cover and non-forest landscape heterogeneity modulate pollination of tropical understory plants. Landsc Ecol 37, 393–409 (2022). https://doi.org/10.1007/s10980-021-01356-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10980-021-01356-x