Contribuição e perspectivas para a biodiversidade, uso sustentável, conservação e serviços ambientais

<Voltar

A polinização no contexto da paisagem: o que de fato sabemos e o que precisamos saber

Resumo

Diversos estudos realizados na última década, principalmente em países de clima temperado, têm demonstrado que a perda de habitat e sua fragmentação provocam alterações na riqueza, composição, abundância e comportamento dos polinizadores. Tais alterações na estrutura das paisagens são consideradas as principais causas da limitação dos “serviços” de polinização nos sistemas agrícolas. A compilação dos resultados desses estudos permite identificar padrões gerais e lacunas no conhecimento que poderão ser utilizados para subsidiar a elaboração de diretrizes para conservação de polinizadores e recuperação de paisagens degradadas.

Abstract

Several studies in the past decade, mostly in temperate countries, has shown that habitat loss and fragmentation cause changes in species richness, composition, abundance and behavior of pollinators. Such changes in the structure of the landscapes are considered the main causes of limitation of pollination service in agricultural systems. The compilation of the results of these studies can identify general patterns and gaps in knowledge that could be used to subsidize the development of public policies for pollinator conservation and restoration of degraded landscapes.

Autores

Dra. Blandina Felipe Viana é Professora no Instituto de Biologia da Universidade Federal da Bahia. E-mail: blandefv@ufba.br
Dr. Danilo Boscolo é Professor na Universidade Federal de São Paulo, Campus Diadema. E-mail: danilo.boscolo@gmail.com
Dr. Eduardo Mariano é Professor do Instituto de Biologia da Universidade Federal da Bahia E-mail: marianon@gmail.com
Dr. Luciano Elsinor Lopes é Professor do Centro de Ciências Biológicas e da Saúde, Departamento de Hidrobiologia da Universidade Federal de São Carlos. E-mail: luciano@gaiasocial.org.br
Dra. Ariadna Lopes é Professora do Centro de Ciências Biológicas da Universidade Federal de Pernambuco. E-mail:avflopes@yahoo.com
MSc. Patrícia Alves Ferreira é Doutorando pelo Programa de Pós-Graduação em Ecologia da Universidade Federal da Bahia. E-mail: patybio13@yahoo.com.br
Dra. Camila Magalhães Pigozzo é Professora do Curso de Ciências Biológicas da Universidade Jorge Amado, Bahia. E-mail: camilapigozzo@yahoo.com.br
Dr. Luis Primo é Pós-Doutorando pelo Instituto de Biologia da Universidade Federal da Bahia. E-mail: luiprimo@yahoo.com.br

Referências

AGUILAR, R.; ASHWORTH, L.; GALETTO, L.; AIZEN, M. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta analysis. Ecology Letters, v. 9, n. 8, p. 968-980, 2006.

AIZEN, M.; FEINSINGER, P. Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology, v. 75, n. 2, p. 330-351, 1994a.

______. Habitat fragmentation, native insect pollinators, and feral honey bees in Argentine 'Chaco Serrano'. Ecological Applications, v. 4, n. 2, p. 378-392, 1994b.

AIZEN, M.; GARIBALDI, L.; CUNNINGHAM, S.; KLEIN, A. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Annals of Botany, v. 103, n. 9, p. 1579, 2009.

ALBRECHT, M.; DUELLI, P.; MULLER, C.; KLEIJN, D.; SCHMID, B. The Swiss agri-environment scheme enhances pollinator diversity and plant reproductive success in nearby intensively managed farmland. Journal of Applied Ecology, v. 44, n. 4, p. 813-822, 2007.

ANDERSSON, E.; BARTHEL, S.; AHRNE, K. Measuring social-ecological dynamics behind the generation of ecosystem services. Ecological Applications, v. 17, n. 5, p. 1267-1278, 2007.

ANDRÉN, H. Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos, v. 71, n. 3, p. 355-366, 1994.

BARLOW, J. et al. Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proceedings of the National Academy of Sciences of the United States of America, v. 104, n. 47, p. 18555-18560, 2007.

BARRETO, L.; RIBEIRO, M.; VELDKAMP, A.; VAN EUPEN, M.; KOK, K.; PONTES, E. Exploring effective conservation networks based on multi-scale planning unit analysis. A case study of the Balsas sub-basin, Maranhão State, Brazil. Ecological Indicators, 2010.

BEIER, P.; VAN DRIELEN, M.; KANKAM, B. Avifaunal collapse in West African forest fragments. Conservation Biology, v. 16, n. 4, p. 1097-1111, 2002.

BERNARD, E.; FENTON, M. Bats in a fragmented landscape: species composition, diversity and habitat interactions in savannas of Santarém, Central Amazonia, Brazil. Biological Conservation, v. 134, n. 3, p. 332-343, 2007.

BITTENCOURT, J.; SEBBENN, A. Patterns of pollen and seed dispersal in a small, fragmented population of the wind-pollinated tree Araucaria angustifolia in southern Brazil. Heredity, v. 99, n. 6, p. 580-591, 2007.

BORGES, L.; SOBRINHO, M.; LOPES, A. Phenology, pollination, and breeding system of the threatened tree Caesalpinia echinata Lam.(Fabaceae), and a review of studies on the reproductive biology in the genus. Flora, v. 204, n. 2, p. 111-130, 2009.

BROSI, B. J.; DAILY, G. C.; EHRLICH, P. R. Bee community shifts with landscape context in a tropical countryside. Ecological Applications, v. 17, n. 2, p. 418-430, 2007.

BRYS, R.; JACQUEMYN, H.; ENDELS, P.; VAN ROSSUM, F.; HERMY, M.; TRIEST, L.; DE BRUYN, L.; BLUST, G. Reduced reproductive success in small populations of the self incompatible Primula vulgaris. Journal of Ecology, v. 92, n. 1, p. 5-14, 2004.

BUCHMANN, S.; NABHAN, G. The Pollination Crisis: The plight of the honey bee and the decline of other pollinators imperils future harvests. Science, v. 36, n. 4, p. 22-27, 1996.

CHACOFF, N.; AIZEN, M. Edge effects on flower visiting insects in grapefruit plantations bordering premontane subtropical forest. Journal of Applied Ecology, v. 43, n. 1, p. 18-27, 2006.

CLERGEAU, P.; BUREL, F. The role of spatio-temporal patch connectivity at the landscape level: an example in a bird distribution. Landscape and Urban Planning, v. 38, n. 1-2, p. 37-43, 1997.

DE MARCO, P.; COELHO, F. M. Services performed by the ecosystem: forest remnants influence agricultural cultures' pollination and production. Biodiversity and Conservation, v. 13, n. 7, p. 1245-1255, 2004.

DEVELEY, P.; STOUFFER, P. Effects of roads on movements by understory birds in mixed species flocks in Central Amazonian Brazil. Conservation Biology, v. 15, n. 5, p. 1416-1422, 2001.

DICK, C. W.; ETCHELECU, G.; AUSTERLITZ, F. Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Molecular Ecology, v. 12, n. 3, p. 753-764, 2003.

DIXON, K. W. Pollination and Restoration. Science, v. 325, n. 5940, p. 571-573, 2009.

DONALDSON, J.; NÄNNI, I.; ZACHARIADES, C.; KEMPER, J. Effects of habitat fragmentation on pollinator diversity and plant reproductive success in renosterveld shrublands of South Africa. Conservation Biology, v. 16, n. 5, p. 1267-1276, 2002.

EKROOS, J.; PIHA, M.; TIAINEN, J. Role of organic and conventional field boundaries on boreal bumblebees and butterflies. Agriculture Ecosystems & Environment, v. 124, n. 3-4, p. 155-159, 2008.

FAHRIG, L. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, v. 34, p. 487-515, 2003.

FORUP, M. L.; HENSON, K. S. E.; CRAZE, P. G.; MEMMOTT, J. The restoration of ecological interactions: plant-pollinator networks on ancient and restored heathlands. Journal of Applied Ecology, v. 45, n. 3, p. 742-752, 2008.

GATHMANN, A.; TSCHARNTKE, T. Foraging ranges of solitary bees. Journal of Animal Ecology, v. 71, n. 5, p. 757-764, 2002.

GEMMILL-HERREN, B.; OCHIENG, A. Role of native bees and natural habitats in eggplant (Solanum melongena) pollination in Kenya. Agriculture, Ecosystems & Environment, v. 127, n. 1-2, p. 31-36, 2008.

GHAZOUL, J.; MCLEISH, M. Reproductive ecology of tropical forest trees in logged and fragmented habitats in Thailand and Costa Rica. Plant Ecology, v. 153, n. 1-2, p. 335-345, 2001.

GIRÃO, L.; LOPES, A.; TABARELLI, M.; BRUNA, E. Changes in tree reproductive traits reduce functional diversity in a fragmented Atlantic forest landscape. PLoS One, v. 2, n. 9, p. 908, 2007.

GONZÁLEZ-VARO, J.; ARROYO, J.; APARICIO, A. Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biological Conservation, v. 142, n. 5, p. 1058-1065, 2009.

GOVERDE, M.; SCHWEIZER, K.; BAUR, B.; ERHARDT, A. Small-scale habitat fragmentation effects on pollinator behaviour: experimental evidence from the bumblebee Bombus veteranus on calcareous grasslands. Biological Conservation, v. 104, n. 3, p. 293-299, 2002.

GREENLEAF, S. S.; KREMEN, C. Wild bees enhance honey bees' pollination of hybrid sunflower. Proceedings of the National Academy of Sciences of the United States of America, v. 103, n. 37, p. 13890-13895, 2006.

HADLEY, A.; BETTS, M. Tropical deforestation alters hummingbird movement patterns. Biology Letters, v. 5, n. 2, p. 207, 2009.

HIRSCH, M.; PFAFF, S.; WOLTERS, V. The influence of matrix type on flower visitors of Centaurea jacea L. Agriculture, Ecosystems & Environment, v. 98, n. 1-3, p. 331-337, 2003.

HOLZSCHUH, A.; STEFFAN-DEWENTER, I.; TSCHARNTKE, T. Agricultural landscapes with organic crops support higher pollinator diversity. Oikos, v. 117, n. 3, p. 354-361, 2008.

______. How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids? Journal of Animal Ecology, v. 79, n. 2, p. 491-500, 2010.

JULES, E.; SHAHANI, P. A broader ecological context to habitat fragmentation: Why matrix habitat is more important than we thought. Journal of Vegetation Science, v. 14, n. 3, p. 459-464, 2003.

KEARNS, C. A.; INOUYE, D. W.; WASER, N. M. Endangered mutualisms: The conservation of plant-pollinator interactions. Annual Review of Ecology and Systematics, v. 29, p. 83-112, 1998.

KLEIN, A.; CUNNINGHAM, S.; BOS, M.; STEFFAN-DEWENTER, I. Advances in pollination ecology from tropical plantation crops. Ecology, v. 89, n. 4, p. 935-943, 2008.

KLEIN, A.; STEFFAN-DEWENTER, I.; TSCHARNTKE, T. Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of the Royal Society of London Series B-Biological Sciences, v. 270, n. 1518, p. 955-961, 2003.

KLEIN, A.; VAISSIERE, B.; CANE, J.; STEFFAN-DEWENTER, I.; CUNNINGHAM, S.; KREMEN, C.; TSCHARNTKE, T. Importance of pollinators in changing landscapes for world crops. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, v. 274, n. 1608, p. 303-313, 2007.

KNIGHT, M. E.; OSBORNE, J. L.; SANDERSON, R. A.; HALE, R. J.; MARTIN, A. P.; GOULSON, D. Bumblebee nest density and the scale of available forage in arable landscapes. Insect Conservation and Diversity, v. 2, n. 2, p. 116-124, 2009.

KOLB, A. Habitat fragmentation reduces plant fitness by disturbing pollination and modifying response to herbivory. Biological Conservation, v. 141, n. 10, p. 2540-2549, 2008.

KREMEN, C. Managing ecosystem services: what do we need to know about their ecology? Ecology Letters, v. 8, n. 5, p. 468-479, 2005.

KREMEN, C. et al. Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecology Letters, v. 10, n. 4, p. 299-314, 2007.

KREMEN, C.; WILLIAMS, N. M.; BUGG, R. L.; FAY, J. P.; THORP, R. W. The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecology Letters, v. 7, n. 11, p. 1109-1119, 2004.

KREMEN, C.; WILLIAMS, N. M.; THORP, R. W. Crop pollination from native bees at risk from agricultural intensification. Proceedings of the Nationa Academy of USA, v. 99, n. 26, p. 16812-16816, 2002.

KREYER, D.; OED, A.; WALTHER-HELLWIG, K.; FRANKL, R. Are forests potential landscape barriers for foraging bumblebees? Landscape scale experiments with Bombus terrestris agg. and Bombus pascuorum (Hymenoptera, Apidae). Biological Conservation, v. 116, n. 1, p. 111-118, 2004.

LAURANCE, W. F. et al. Ecosystem decay of Amazonian forest fragments: A 22-year investigation. Conservation Biology, v. 16, n. 3, p. 605-618, 2002.

LENNARTSSON, T. Extinction thresholds and disrupted plant-pollinator interactions in fragmented plant populations. Ecology, v. 83, n. 11, p. 3060-3072, 2002.

LONSDORF, E.; KREMEN, C.; RICKETTS, T.; WINFREE, R.; WILLIAMS, N.; GREENLEAF, S. Modelling pollination services across agricultural landscapes. Annals of Botany, v. 103, n. 9, p. 1589-1600, 2009.

LOPES, A.; GIRÃO, L.; SANTOS, B.; PERES, C.; TABARELLI, M. Long-term erosion of tree reproductive trait diversity in edge-dominated Atlantic forest fragments. Biological Conservation, v. 142, n. 6, p. 1154-1165, 2009.

LOPES, L. E.; BUZATO, S. Variation in pollinator assemblages in a fragmented landscape and its effects on reproductive stages of a self-incompatible treelet, Psychotria suterella (Rubiaceae). Oecologia, v. 154, p. 305-314, 2007.

METZGER, J. Tree functional group richness and landscape structure in a Brazilian tropical fragmented landscape. Ecological Applications, v. 10, n. 4, p. 1147-1161, 2000.

______. O que é ecologia de paisagens. Biota Neotropica, v. 1, n. 1, p. 1-9, 2001.

METZGER, J.; DÉCAMPS, H. The structural connectivity threshold: an hypothesis in conservation biology at the landscape scale. Acta Oecologica, v. 18, n. 1, p. 1-12, 1997.

MEYER, B.; JAUKER, F.; STEFFAN-DEWENTER, I. Contrasting resource-dependent responses of hoverfly richness and density to landscape structure. Basic and Applied Ecology, v. 10, n. 2, p. 178-186, 2009.

MILET-PINHEIRO, P.; SCHLINDWEIN, C. Do euglossine males (Apidae, Euglossini) leave tropical rainforest to collect fragrances in sugarcane monocultures? Revista Brasileira de Zoologia, v. 22, p. 853-858, 2005.

MORATO, E.; CAMPOS, L. Efeitos da fragmentação florestal sobre vespas e abelhas solitárias em uma área da Amazônia Central. Revista Brasileira de Zoologia, v. 17, n. 2, p. 429-444, 2000.

MOURA, D.; SCHLINDWEIN, C. Mata ciliar do rio São Francisco como biocorredor para Euglossini (Hymenoptera, Apidae) de Florestas Tropicais Úmidas. Neotropical Entomology, v. 38, n. 2, p. 281-284, 2009.

MURCIA, C. Edge effects in fragmented forests: implications for conservation. Trends in Ecology & Evolution, v. 10, n. 2, p. 58-62, 1995.

OSBORNE, J.; CLARK, S.; MORRIS, R.; WILLIAMS, I.; RILEY, J.; SMITH, A.; REYNOLDS, D.; EDWARDS, A. A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. Journal of Applied Ecology, v. 36, n. 4, p. 519-533, 1999a.

OSBORNE, J. L.; CLARK, S. J.; MORRIS, R. J.; WILLIAMS, I. H.; RILEY, J. R.; SMITH, A. D.; REYNOLDS, D. R.; EDWARDS, A. S. A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. Journal of Applied Ecology, v. 36, n. 4, p. 519-533, 1999b.

POWELL, A. H.; POWELL, G. V. N. Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica, v. 19, n. 2, p. 176-179, 1987.

RENJIFO, L. Effect of natural and anthropogenic landscape matrices on the abundance of subandean bird species. Ecological Applications, v. 11, n. 1, p. 14-31, 2001.

RICKETTS, T. H.; DAILY, G. C.; EHRLICH, P. R.; MICHENER, C. D. Economic value of tropical forest to coffee production. Proceedings of the National Academy of Sciences of the United States of America, v. 101, n. 34, p. 12579-12582, 2004.

RICKETTS, T. H. et al. Landscape effects on crop pollination services: are there general patterns? Ecology Letters, v. 11, n. 5, p. 499-515, 2008.

SJÖDIN, N.; BENGTSSON, J.; EKBOM, B. The influence of grazing intensity and landscape composition on the diversity and abundance of flower visiting insects. Journal of Applied Ecology, v. 45, n. 3, p. 763-772, 2008.

SMITH, J.; HELLMANN, J. Population persistence in fragmented landscapes. Trends in Ecology & Evolution, v. 17, n. 9, p. 397-399, 2002.

STEFFAN-DEWENTER, I.; MÜNZENBERG, U.; TSCHARNTKE, T. Pollination, seed set and seed predation on a landscape scale. Proceedings of the Royal Society of London. Series B: Biological Sciences, v. 268, n. 1477, p. 1685-1690, 2001.

STEFFAN-DEWENTER, I.; POTTS, S. G.; PACKER, L. Pollinator diversity and crop pollination services are at risk. Trends in Ecology & Evolution, v. 20, n. 12, p. 651-652, 2005.

STEFFAN-DEWENTER, I.; TSCHARNTKE, T. Effects of habitat isolation on pollinator communities and seed set. Oecologia, v. 121, n. 3, p. 432-440, 1999.

STEFFAN-DEWENTER, I.; WESTPHAL, C. The interplay of pollinator diversity, pollination services and landscape change. Journal of Applied Ecology, v. 45, n. 3, p. 737-741, 2008.

TABARELLI, M.; AGUIAR, A.; GIRÃO, L.; PERES, C.; LOPES, A. Effects of pioneer tree species hyperabundance on forest fragments in Northeastern Brazil. Conservation Biology, v. 24, n. 6, p. 1654–1663, 2010.

TAKI, H.; KEVAN, P. G. Does habitat loss affect the communities of plants and insects equally in plant-pollinator interactions? Preliminary findings. Biodiversity and Conservation, v. 16, n. 11, p. 3147-3161, 2007.

TAYLOR, P.; FAHRIG, L.; HENEIN, K.; MERRIAM, G. Connectivity is a vital element of landscape structure. Oikos, v. 68, n. 3, p. 571-573, 1993.

TOMIMATSU, H.; OHARA, M. Effects of forest fragmentation on seed production of the understory herb Trillium camschatcense. Conservation Biology, v. 16, n. 5, p. 1277-1285, 2002.

TONHASCA, A.; ALBUQUERQUE, G.; BLACKMER, J. Dispersal of euglossine bees between fragments of the Brazilian Atlantic Forest. Journal of Tropical Ecology, v. 19, n. 01, p. 99-102, 2003.

TONHASCA, A.; BLACKMER, J. L.; ALBUQUERQUE, G. S. Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic forest. Biotropica, v. 34, n. 3, p. 416-422, 2002a.

______. Within-habitat heterogeneity of euglossine bee populations: a re-evaluation of the evidence. Journal of Tropical Ecology, v. 18, n. 06, p. 929-933, 2002b.

TSCHARNTKE, T.; BOMMARCO, R.; CLOUGH, Y.; CRIST, T. O.; KLEIJN, D.; RAND, T. A.; TYLIANAKIS, J. M.; VAN NOUHUYS, S.; VIDAL, S. Conservation biological control and enemy diversity on a landscape scale. Biological Control, v. 43, n. 3, p. 294-309, 2007.

TSCHARNTKE, T.; BRANDL, R. Plant-insect interactions in fragmented landscapes. Annual Reviews in Entomology, v. 49, n. 1, p. 405-430, 2004.

TSCHARNTKE, T.; KLEIN, A.; KRUESS, A.; STEFFAN-DEWENTER, I.; THIES, C. Landscape perspectives on agricultural intensification and biodiversity–ecosystem service management. Ecology Letters, v. 8, n. 8, p. 857-874, 2005.

TSCHARNTKE, T.; SEKERCIOGLU, C. H.; DIETSCH, T. V.; SODHI, N. S.; HOEHN, P.; TYLIANAKIS, J. M. Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology, v. 89, n. 4, p. 944-951, 2008.

WESTPHAL, C.; STEFFAN-DEWENTER, I.; TSCHARNTKE, T. Mass flowering crops enhance pollinator densities at a landscape scale. Ecology Letters, v. 6, n. 11, p. 961-965, 2003.

WIENS, J. Habitat fragmentation: island v landscape perspectives on bird conservation. Ibis, v. 137, n. s1, p. S97-S104, 1995.

WINFREE, R.; AGUILAR, R.; VÁZQUEZ, D.; LEBUHN, G.; AIZEN, M. A meta-analysis of bees' responses to anthropogenic disturbance. Ecology, v. 90, n. 8, p. 2068-2076, 2009.

YAMAMOTO, L.; KINOSHITA, L.; MARTINS, F. Síndromes de polinização e de dispersão em fragmentos da Floresta Estacional Semidecídua Montana, SP, Brasil. Acta Botanica Brasilica, v. 21, n. 3, p. 553-573, 2007.

ZANETTE, L. R. S.; MARTINS, R. P.; RIBEIRO, S. P. Effects of urbanization on Neotropical wasp and bee assemblages in a Brazilian metropolis. Landscape and Urban Planning, v. 71, n. 2-4, p. 105-121, 2005.