Seasonal Variation in Bee-Plant Interactions in an Inselberg in the Atlantic Forest in Southeastern Brazil

Marcelita França Marques, Mariana Scaramussa Deprá, Maria Cristina Gaglianone

Abstract


Studies on bee-plant interactions are relevant to the understanding of temporal patterns in neotropical communities. In isolated habitats such as inselbergs little is yet known about the temporal dynamics in the availability of fl oral resources and interacting bee. In the present study, the objective is to verify the eff ect of seasonality on the bee-plant interaction in an Atlantic Forest inselberg in southeastern Brazil. The bees were sampled monthly in the dry (April/2008-September/2008) and wet seasons (October/2008-March/2009) using an entomological net. A total of 322 bees of 33 species were captured on fl owers of 34 species of plants during the year. Bees richness was similar between seasons (22 species in the wet season and 21 in the dry season), but abundance was higher in the wet season (60% of individuals) and higher diversity occurred in the dry season. Augochloropsis sp1 were the most abundant species and visited the largest number of plant species at each season. In the interaction network, plants with the highest degree were distinct between the seasons. The number of possible interactions was higher in the dry season compared to the wet season and connectance was similar; nestedness however varied between the seasons. The composition of plant and bees species was distinct between the seasons, as well as the interactions between them, mainly due to the alteration in the composition of the plant species and the change in the choice of the bees for the floral resources between the seasons.


Keywords


Floral Visitors, Seasonality, Semidecidual Forest, Ecological Networks

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References


Aguiar, C.M.L. & Zanella, F.C.V. (2005). Estrutura da Comunidade de Abelhas (Hymenoptera: Apoidea: Apiformis) de uma Área na Margem do Domínio da Caatinga (Itatim, BA). Neotropical Entomology, 34: 15-24. doi: 10.1590/S1519-566X2005000100003

Aguiar, W.M. & Gaglianone, M.C. (2011). Euglossine bees (Hymenoptera Apidae Euglossina) on an inselberg in the Atlantic Forest domain of southeastern Brazil. Tropical Zoology, 24: 107-125.

Almeida-Neto, M.P., Guimarães, P.R., Guimarães, R., Loyola, D. & Ulrich, W. (2008). A consistente metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos, 117: 1227-1239. doi: 10.1111/j.2008.0030-1299.16644.x

APG III. (2009). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society, 161: 105-121.

Barabási, A.L. & Albert, R. (1999). Emergence of Scaling in Random Networks. Science, 286: 509-512. doi: 10.1126/science.286.5439.509.

Bascompte, J., Jordano, P., Melian, C.J. & Olesen, M. (2003). The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences, 100: 9383-9387. doi: 10.1073/pnas.1633576100

Batalha-Filho, H., Nunes, L.A., Pereira, D.G. & Waldschmidt, A.M. (2007). Inventário da fauna de abelhas (Hymenoptera, Apoidea) em uma área de caatinga da região de Jequié, BA. Bioscience Journal, 23(1): 24-29.

Bernardino, A.S. & Gaglianone, M.C. (2008). Nest distribution and nesting habits of Xylocopa ordinaria Smith (Hymenoptera, Apidae) in a restinga area in the northern Rio de Janeiro State, Brazil. Revista Brasileira de Entomologia, 52: 434-440. doi: 10.1590/S0085-56262008000300017

Biesmeijer, J.C., Slaa, E.J., Castro, M.S., Viana, B.F., Kleinert, A.M.P. & Imperatriz-Fonseca, V.L. (2005). Connectance of Brazilian social bee – food plant networks is infl uenced by habitat, but not by latitude, altitude or network size. Biota Neotropica, 5: 1-9. doi: 10.1590/S1676-06032005000100010

Burkle, L.A. & Alarcón, R. (2011). The future of plant – pollinator diversity: Understanding interaction networks across time, space, and global change. American Journal of Botany, 98(3): 1-11. doi: 10.3732/ajb.1000391

Carstensen, D., Sabatino, M., Trøjelsgaard, K. & Morellato, L. (2014). Beta Diversity of Plant-Pollinator Networks and the Spatial Turnover of Pairwise Interactions. PLoS ONE, 10(2): e0117763. doi: 10.1371/journal.pone.0112903

Dec, E. & Mouga, D.M.D.S. (2014). Diversidade de abelhas (Hymenoptera: Apidae) em área de mata atlântica em Joinville, Santa Catarina. Acta Biológica Catarinense, 1: 15-27. doi:10.21726/abc.v1i2.91

Deprá, M.S. & Gaglianone, M.C. (2018). Interações entre plantas e polinizadores sob uma perspectiva temporal. Oecologia Australis, 22(1): 1-16. doi: 10.4257/oeco.2018.2201.01

Dupont, Y.L., Padrón, B., Olesen, J.M. & Petanidou, T. (2009). Spatio-temporal variation in the structure of pollination networks. Oikos, 118(8): 1261-1269.

Gröger, A. & Huber, O. (2007). Rock outcrop habitats in the Venezuelan Guayana lowlands: main vegetation types and fl oristic components. Revista Brasileira de Botânica, 30: 599-609. doi: 10.1590/S0100-84042007000400006

Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001). PAST: Paleontological statistical software package for education and data analysis. Palaentologia Electronica, 4 (1): 9.

INMET. (2017). Instituto Nacional de Metereologia. http://inmet.gov.br. (accessed date: 3 March, 2017).

Jordano, P. (1987). Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence, and coevolution. American Naturalist, 129: 657-677.

Jordano, P., Bascompte, J. & Olesen, J.M. (2003) Invariant properties in coevolutionary networks of plant–animal interactions. Ecology Letters, 6: 69-81. doi: 10.1046/j.1461-0248.2003.00403.x

Kaiser-Bunbury, C.N., Vázquez, D.P., Stang, M. & Ghazoul, J. (2014). Determinants of the microstructure of plant–pollinator networks. Ecology, 95 (12): 3314-3324. doi: 10.18 90/14-0024.1

Kemp, J.E., Evans, D.M., Augustyn, W.J. & Ellis, A.G. (2017). Invariant antagonistic network structure despite high spatial and temporal turnover of interactions. Ecography, 40:1-10. doi: 10.1111/ecog.02150

Kleinert, A.M.P., Ramalho, M., Cortopassi-Laurino, M., Ribeiro, M.F. & Imperatriz-Fonseca, V.L. (2009). Abelhas sociais (Bombini, Apini, Meliponini). In A.R. Panizi & J.R.P. Parra (Eds.), Bioecologia e nutrição de insetos: Base para o manejo integrado de pragas (pp. 373-426). Brasília: Embrapa.

Köppen, W. (1948). Climatologia. México: Fondo de Cultura Económica, 478 p.

Marques, M.F. & Gaglianone, M.C. (2008). Biologia de nidificação e variação altitudinal na abundância de Megachile (Melanosarus) nigripennis Spinola (Hymenoptera, Megachilidae) em um inselbergue na Mata Atlântica, Rio de Janeiro. Bioscience Journal, 29(1): 198-208.

Marques, A.P.S., Camargo, R.C.R., Malagodi-Braga, K.S., Ono, E.O. & Urchei, M.A. (2013). Avaliação do potencial melífero e polinífero de Crotalaria juncea L. e Crotalaria spectabilis Roth. (Fabaceae, Papilionoideae). Cadernos de Agroecologia, 8(2): 1-4.

Mauad, L.P., Buturi, F.O.S., Souza, T.P., Nascimento, M.T. & Braga, J.M.A. (2014). New distribution record and implications for conservation of the endangered Wunderlichia azulensis Maguire & G.M. Barroso (Asteraceae: Wunderlichieae). Check List, 10(3): 706-708. doi: 10.15560/10.3.706

Memmott, J., Waser, N.M. & Price, M.V. (2004). Tolerance of pollination networks to species extinctions. Proceeding of the Royal Society of London, 271: 2605-2611. doi: 10.1098/rspb.2004.2909

Morellato, P.C. & Leitão Filho, H.F. (1996). Reproductive phenology of climbers in a Southeastern Brazilian Forest. Biotropica, 28: 180-191. doi: 10.2307/2389073

Moreira, E., Boscolo, D. & Viana, B. (2015). Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLoS ONE, 10: e0123628. doi: 10.1371/journal.pone.0123628

Mouga, D.M.D.S. & Krug, C. (2010). Comunidade de abelhas nativas (Apidae) em Floresta Ombrófi la Densa Montana em Santa Catarina. Zoologia, 27: 70-80.

Murray-Smith, C., Brummitt, C.A., Oliveira-Filho, A.T., Bachman, S., Moat, J., Lughadha, E.M.N. & Lucas, E.J. (2008). Plant Diversity Hotspots in the Atlantic Coastal Forests of Brazil. Conservation Biology, 23: 151-163. doi:

1111/j.1523-1739.2008.01075.x

Novotny, V. (2009). Beta diversity of plant-insect food webs in tropical forest: a conceptual framework. Insect Conservation and Diversity, 2:5-9. doi: 10.1111/j.1752-4598.2008.00035.x

Nunes, Y.R.F., Fagundes, M., Santos, R.M., Domingues, E.B.S., Almeida, H.S. & Nunes, A.P.D.G. (2005). Atividades fenológicas de Guazuma ulmifolia Lam. (Malvaceae) em uma floresta estacional decidual no norte de Minas Gerais. Lundiana, 6: 99-105.

Olesen, J.M., Bascompte, J., Elberling, H. & Jordano, P. (2008). Temporal dynamics in a pollination network. Ecology, 89: 1573-1582. doi: 10.1890/07-0451.1

Pessanha, A.S., Menini Neto, L., Forzza, R.C. & Nascimento, M.T. (2014). Composition and conservation of Orchidaceae on an inselberg in the Brazilian Atlantic Forest and floristic relationships with areas of Eastern Brazil. Revista de BiologiaTropical, 62: 829-841.

Petanidou, T., Kallimanis, A.S., Tzanopoulos, J., Sgardelis, S.P. & Pantis, J.D. (2008). Long-term observation of a pollination network: fl uctuation in species and interactions, relative invariance of network structure and implycations for estimates of specialization. Ecology Letters, 11: 564-575. doi: 10.1111/j.1461-0248.2008.01170.x.

Pimenta, J.A., Rossi, L.B., Torezan, J.M.D., Cavalheiro, A.L. & Bianchini, E. (2011). Produção de serapilheira e ciclagem de nutrientes de um reflorestamento e de uma floresta estacional semidecidual no sul do Brasil. Acta Botanica Brasilica, 25(1): 53-57. Moreira, E., Boscolo, D. & Viana, B. (2015). Spatial

heterogeneity regulates plant-pollinator networks across

multiple landscape scales. PLoS ONE, 10: e0123628. doi:

1371/journal.pone.0123628

Mouga, D.M.D.S. & Krug, C. (2010). Comunidade de abelhas

nativas (Apidae) em Floresta Ombrófi la Densa Montana em

Santa Catarina. Zoologia, 27: 70-80.

Murray-Smith, C., Brummitt, C.A., Oliveira-Filho, A.T.,

Bachman, S., Moat, J., Lughadha, E.M.N. & Lucas, E.J.

(2008). Plant Diversity Hotspots in the Atlantic Coastal

Forests of Brazil. Conservation Biology, 23: 151-163. doi:

1111/j.1523-1739.2008.01075.x

Novotny, V. (2009). Beta diversity of plant-insect food webs in

tropical forest: a conceptual framework. Insect Conservation

and Diversity, 2:5-9. doi: 10.1111/j.1752-4598.2008.00035.x

Nunes, Y.R.F., Fagundes, M., Santos, R.M., Domingues,

E.B.S., Almeida, H.S. & Nunes, A.P.D.G. (2005). Atividades

fenológicas de Guazuma ulmifolia Lam. (Malvaceae) em

uma fl oresta estacional decidual no norte de Minas Gerais.

Lundiana, 6: 99-105.

Olesen, J.M., Bascompte, J., Elberling, H. & Jordano, P.

(2008). Temporal dynamics in a pollination network. Ecology,

: 1573-1582. doi: 10.1890/07-0451.1

Pessanha, A.S., Menini Neto, L., Forzza, R.C. & Nascimento,

M.T. (2014). Composition and conservation of Orchidaceae

on an inselberg in the Brazilian Atlantic Forest and fl oristic

relationships with areas of Eastern Brazil. Revista de Biologia

Tropical, 62: 829-841.

Petanidou, T., Kallimanis, A.S., Tzanopoulos, J., Sgardelis,

S.P. & Pantis, J.D. (2008). Long-term observation of a

pollination network: fl uctuation in species and interactions,

relative invariance of network structure and implycations for

estimates of specialization. Ecology Letters, 11: 564-575. doi:

1111/j.1461-0248.2008.01170.x.

Potts, S.G., Imperatriz-Fonseca, V., Ngo, H.T., Biesmeijer, J.C., Breeze, T.D., Dicks, L.V., Garibaldi, L.A., Hill, R., Settele, J. & Vanbergen, A.J. (2016). The assessment report on pollinators, pollination and food production: summary for policymakers. Germany: Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, 36 p.

Porembski, S., Martinelli, G., Ohlemüller, R. & Barthlott, W. (1998). Diversity and ecology of saxicolous vegetation mats on inselbergs in the Brazilian Atlantic Rainforest. Biodiversity Research, 4: 107-119.

Porembski, S. & Barthlott, W. (2000). Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccationtolerant vascular plants. Plant Ecology, 151: 19-28. doi: 10.1023/A:1026565817218

R Development Core Team. (2016). R: a language and environment for statistical computing, version 3.3.1. R Foundation for Statistical Computing, Computer Program, Vienna

Rech, A.R., Agostini, K., Oliveira, P.E. & Machado, I.C. (2014). Biologia da Polinização. Rio de Janeiro: Ceres Projeto Cultural, 524 p.

Roubik, D.W. (1989). Ecology and natural history of tropical bees. New York: Cambridge University Press, 514 p.

Roubik D.W. & Hanson P.E. (2004). Orchids bees of tropical America: biology and field guide. Costa Rica: INBio Press, 370 p.

Santos, G.M.M., Delabie, J.H.C. & Resende, J.J. (1999). Caracterização da mirmecofauna (Hymenoptera – Formicidae) associada à vegetação periférica de inselbergs (Caatinga- Arbórea- estacional-Semi Decidua) em Itatim - Bahia - Brasil. Sitientibus, 20: 33-43.

Santos, K., Kinoshita, L.S. & Rezende, A.A. (2009). Species composition of climbers in seasonal semideciduous forest fragments of Southeastern Brazil. Biota Neotropica, 9: 175-188. doi: 10.1590/S1676-06032009000400018

Santos, G., Dáttilo, W. & Presley, S. (2014). The seasonal dynamic of ant-fl ower networks in a semi-arid tropical environment. Ecological Entomology, 39: 674-683. doi:10.1111/een.12138.

Sargent, R.S. & Ackerly, D.D. (2008). Plant–pollinator interactions and the assembly of plant communities. Trends in Ecology and Evolution, 23: 123-130. doi: 10.1016/j.tree.2007.11.003.

Silva, W., Guimarães-Jr, P.R., Reis, S.F. & Guimarães, P. (2007). Investigating fragility in plantfrugivore networks: a case study for Atlantic Forest. In A.J. Dennis, R. Green, E.W. Schupp & D. Wescott (Eds.), Frugivory and seed dispersal: theory and applications in a changing world (pp. 561-578). Wallingford: Commonwealth Agricultural Bureau International.

Silva, J.B. (2016). Panorama sobre a vegetação em afl oramentos rochosos do Brasil. Oecologia Australis, 20:451-463. doi: 10.4257/oeco.2016.2004.05

Teixeira, F.M., Schwartz, T.A.C & Gaglianone, M.C. (2011). Biologia da Nidificação de Megachile (Moureapis) benigna Mitchell. EntomoBrasilis, 4(3): 92-99.




DOI: http://dx.doi.org/10.13102/sociobiology.v65i4.3473

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