Structure of ant-diaspore networks and their functional outcomes in a Brazilian Atlantic Forest

Authors

  • Bianca Ferreira da Silva Laviski Universidade Federal Rural do Rio de Janeiro
  • Antonio José Mayhé-Nunes Universidade Federal Rural do Rio de Janeiro
  • André Felippe Nunes-Freitas Universidade Federal Rural do Rio de Janeiro

DOI:

https://doi.org/10.13102/sociobiology.v68i3.7104

Keywords:

Ant-fruit interactions, secondary dispersal, seed cleaning, seed removal, mutualistic networks

Abstract

Ants are able to interact with fruits and seeds that are not adapted for ant seed dispersal. In Brazil, several studies show interactions of ants with non-myrmecochorous diaspores; however, few of them have studied the structure of ant-fruit networks. The use of the network approach allows visualising multiple interactions between partners and how they are shaped by the community context. Our study aims to investigate ant-fruit networks as well as quantitative and qualitative dispersal components in a fragment of the Brazilian Atlantic Forest. We investigated the structure of interaction networks, diaspore removal rates, diaspore destination and dispersal distance over two years of observation. We constructed three interaction networks: dry season, rainy season and total, with the latter comprising the two formers. The diaspore removal rate, dispersal distance and diaspore destination experiments were performed for the plant species Miconia calvescens, Miconia prasina, Psychotria leiocarpa and Inga edulis. We recorded a large number of interactions, with diaspore cleaning being more frequent than removal. Ant-diaspore networks were nested, non-modular and little specialized. M. calvescens, M. prasina and I. edulis showed higher diaspore removal rates. Diaspore removal distances were the same among M. calvescens, M. prasina and I. edulis. In M. calvescens and I. edulis, the main diaspore destination was the ant’s nest. Our study shows that diaspore cleaning is the most common behavior in ant-diaspore interactions and there are no differences in the organization of interaction networks over the seasons. These results have implications for the future structure of plant communities, considering that a small part of the diaspores is removed, and that most of them are cleaned, favouring germination at the deposition site.

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Author Biographies

Antonio José Mayhé-Nunes, Universidade Federal Rural do Rio de Janeiro

Departamento de Biologia Animal

André Felippe Nunes-Freitas, Universidade Federal Rural do Rio de Janeiro

Departamento de Ciências Ambientais

References

Almeida, F.S., Mayhé-Nunes, A.J. & Queiroz, J.M. (2013) The Importance of Poneromorph Ants for Seed Dispersal in Altered Environments. Sociobiology, 60: 229–235. doi:10.13102/sociobiology.v60i3.229-235

Almeida-Neto, M., Guimarães-Jr, P.R., Lewinsohn, T. (2007) On nestedness analyses: rethinking matrix temperature and anti-nestedness. Oikos, 116: 716-722. doi: 10.1111/j.0030-1299.2007.15803.x

Anjos, D., Dáttilo, W. & Del-Claro, K. (2018) Unmasking the architecture of ant-diaspore networks in the Brazilian Savanna. PLoS ONE, 13: e0201117. doi: 10.1371/journal.pone.0201117

Baccaro, F.B., Feitosa, R.M., Fernández, F., Fernandes, I.O., Izzo, T.J., Souza, J.L.P. & Solar, R. (2015) Guia para os gêneros de formigas do Brasil. Manaus: INPA, 388 p

Bascompte, J. (2007) Networks in ecology. Basic and Applied Ecology, 8: 485-490. doi: 10.1016/j.baae.2007.06.003

Bascompte, J. & Jordano, P. (2007) Plant-Animal Mutualistic Networks: The Architecture of Biodiversity. Annual Review of Ecology, Evolution, and Systematics, 38: 567–593. doi: 10.1146/annurev.ecolsys.38.091206.095818

Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003) The nested assembly of plant-animal mutualistic networks. PNAS, 100: 9383-9387. doi: 10.1073/pnas.1633576100

Bascompte, J., Jordano, P. & Olesen, J. M. (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science, 312: 431–433. doi: 10.1126/science.1123412

Beattie, A.J. (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge: Cambridge University Press, 182 p

Bieber, A.G.D., Silva, P.S.D., Sendoya, S.F. & Oliveira, P.S. (2014) Assessing the impact of deforestation of the Atlantic rainforest on ant-fruit interactions: A field experiment using synthetic fruits. PLoS ONE, 9: e90369. doi: 10.1371/journal.pone.0090369

Blüthgen, N. (2011) Interações planta-animais e a importância funcional da biodiversidade. In K. Del-Claro & H.M. Torezan-Siligardi (Orgs.), Ecologia das Interações Plantas-Animais: uma abordagem ecológico-evolutiva (pp. 259-272). Rio de Janeiro: Technical Books.

Byrne, M.M. & Levey, D.J. (1993) Removal of seeds from frugivore defecations by ants in a Costa Rican rain forest. Vegetatio, 107: 363-374. doi: 10.1007/BF00052235

Camargo, P.H.S.A., Martins, M.M., Feitosa, R.M. & Christianini, A.V. (2016) Bird and ant synergy increases the seed dispersal effectiveness of an ornithochoric shrub. Oecologia, 181: 507-518. doi: 10.1007/s00442-016-3571-z

Camargo, P.H.S.A., Rodrigues, S.B.M., Piratelli, A.J., Oliveira, P.S. & Christianini, A.V. (2019) Interhabitat variation in diplochory : Seed dispersal effectiveness by birds and ants differs between tropical forest and savanna. Perspectives in Plant Ecology, Evolution and Systematics, 38: 48–57. doi: 10.1016/j.ppees.2019.04.002

Christianini, A.V., Mayhé-Nunes, A.J. & Oliveira, P.S. (2007) The role of ants in the removal of non-myrmecochorous diaspores and seed germination in a neotropical savanna. Journal of Tropical Ecology, 23: 343–351. doi: 10.1017/S0266467407004087

Christianini, A.V., Mayhé-Nunes, A.J. & Oliveira, P.S. (2012) Exploitation of Fallen Diaspores by Ants: Are there Ant-Plant Partner Choices? Biotropica, 44: 360-367. doi:10.1111/j.1744-7429.2011.00822.x

Christianini, A.V. & Oliveira, P.S. (2010) Birds and ants provide complementary seed dispersal in a neotropical savanna. Journal of Ecology, 98: 573-582. doi: 10.1111/j.1365-2745.2010.01653.x

Conde, M.M.S., Lima, H.R.P. & Peixoto, A.L. (2005) Aspectos florísticos e vegetacionais da Marambaia, Rio de Janeiro, Brasil. In L.F.T. Menezes, A.L. Peixoto & D.S.D. Araújo (Eds.), História Natural da Marambaia (pp. 133-168). Seropédica: EDUR.

Dáttilo, W., Guimarães, P.R. & Izzo, T.J. (2013) Spatial structure of ant-plant mutualistic networks. Oikos, 122: 1643-1648. doi: 10.1111/j.1600-0706.2013.00562.x

Dáttilo, W., Izzo, T.J., Vasconcelos, H.L. & Rico-Gray, V. (2013) Strength of the modular pattern in Amazonian symbiotic ant-plant networks. Arthropod-Plant Interactions, 7: 455-461. doi: 10.1007/s11829-013-9256-1

Dáttilo, W., Rico-Gray, V., Rodrigues, D.J. & Izzo, T.J. (2013) Soil and vegetation features determine the nested pattern of ant-plant networks in a tropical rainforest. Ecological Entomology, 38: 374-380. doi: 10.1111/een.12029

Dáttilo, W., Díaz-Castelazo, C. & Rico-Gray, V. (2014) Ant dominance hierarchy determines the nested pattern in ant-plant networks. Biological Journal of the Linnean Society, 113: 405-414. doi: 10.1111/bij.12350

Dáttilo, W., Fagundes, R., Gurka, C.A.Q., Silva, M.S.A., Vieira, M.C.L., Izzo, T.J., Díaz-Castelazo, C., Del-Claro, K. & Rico-Gray, V. (2014) Individual-based ant-plant networks: diurnal-nocturnal structure and species-area relationship. PLoS One, 9: e99838. doi:10.1371/journal.pone.0099838

Dáttilo, W., Marquitti, F.M.D., Guimarães, P.R. & Izzo T.J. (2014) The structure of ant-plant ecological networks: is abundance enough? Ecology, 95: 475-485. doi: 10.1890/12-1647.1

Delabie, J.H.C., Ospina, M. & Zabala, G. (2003) Relaciones entre hormigas y plantas. In F. Fernandez (Ed.), Introducción a las hormigas de la región Neotropical (pp. 167-180). Bogotá: Instituto de Investigación de Recursos Biológicos Alexander von Humboldt.

Díaz-Castelazo, C., Sánchez-Galván, I.R., Guimarães-Jr, P.R., Raimundo, R.L.G & Rico-Gray, V. (2013) Long-term temporal variation in the organization of an ant-plant network. Annals of Botany, 111: 1285-1293. doi:10.1093/aob/mct071

Farji-Brener, A.G. & Medina, C.A. (2000) The importance of where to dump the refuse: seed banks and fine roots in nests of the leaf-cutting ants Atta cephalotes and A. colombica. Biotropica, 32: 120-126. doi:10.1111/j.1744-7429.2000.tb00454.x

Fedriani, J.M. & Wiegand, T. (2014) Hierarchical mechanisms of spatially contagious seed-dispersal networks. Ecology, 95: 514–526. doi: 10.1890/13-0718.1

Gallegos, S.C., Hensen, I. & Schleuning, M. (2014) Secondary dispersal by ants promotes forest regeneration after deforestation. Journal of Ecology, 102: 659-666. doi:10.1111/1365-2745.12226

Giannini, T.C., Garibaldi, L.A., Acosta, A.L., Silva, J.S., Maia, K.P., Saraiva, A.M., Guimarães, P.R. & Kleinert, A.M.P. (2015) Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS ONE, 10: e0137198. doi: 10.1371/journal.pone.0137198

Giladi, I. (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos, 112: 481-492. doi: 10.1111/j.0030-1299.2006.14258.x

Goés, M.H.B., Silva, J.X., Rodrigues, A.F., Cavalcante, M.S.G., Roncarati, H., Cravo, C.D., Menezes, L.F.T., Anjos, L.H., Valadares, G.S. & Pereira, M.G. (2005) Modelo digital para a restinga e paleoilha da Marambaia, Rio de Janeiro. In L.F.T. Menezes, A.L. Peixoto & D.S.D. Araújo (Eds.), História Natural da Marambaia (pp. 231-284). Seropédica: EDUR.

Gómez, C. & Espadaler, X. (2013) An update of the world survey of myrmecochorous dispersal distances. Ecography, 36: 1193-1201. doi: 10.1111/j.1600-0587.2013.00289.x

Gorb, E. & Gorb, S. (2000) Effects of seed aggregation on the removal rates of elaiosome-bearing Chelidonium majus and Viola odourata seeds carried by Formica polyctena ants. Ecological Research, 15: 187-192. doi: 10.1046/j.1440-1703.2000.00338.x

Guimarães-Jr, P.R. & Cogni, R. (2002) Seed cleaning of Cupania vernalis (Sapindaceae) by ants: edge effect in a highland forest in south-east Brazil. Journal of Tropical Ecology, 18: 303-307. doi: 10.1017/S0266467402002213

Guimarães-Jr, P.R. & Guimarães, P. (2006) Improving the analyses of nestedness for large sets of matrices. Environmental Modelling & Software, 21: 1512-1513. doi:10.1016/j.envsoft.2006.04.002

Guimarães-Jr, P.R., Rico-Gray, V., Oliveira, P.S., Izzo, T.J., Reis, S.F. & Thompson, J.N. (2007) Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Current Biology, 17: 1797-1803. doi: 10.1016/j.cub.2007.09.059

Guimerá, R. & Amaral, L.A.N. (2005) Cartography of complex networks: modules and universal roles. Journal of Statistical Mechanics, P02001: P02001-1–P02001-13. doi:10.1088/1742-5468/2005/02/P02001

Janzen, D.H. (1970) Herbivores and the number of tree species in tropical forests. The American Naturalist, 104: 501 – 528.

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

Kaspari, M. (1993) Removal of seeds from Neotropical frugivore droppings: Ant responses to seed number. Oecologia, 95: 81-88. doi: 10.1007/BF00649510.

Lange, D. & Del-Claro, K. (2014) Ant-Plant Interaction in a Tropical Savanna: May the Network Structure Vary over Time and Influence on the Outcomes of Associations? PLoS ONE, 9: e105574. doi: 10.1371/journal.pone.0105574

Leal, I.R. & Oliveira, P.S. (1998) Interactions between Fungus-Growing Ants (Attini), Fruits and Seeds in Cerrado Vegetation in Southeast Brazil. Biotropica, 30: 170-178. doi: 10.1111/j.1744-7429.1998.tb00052.x

Leal, I.R., Wirth, R. & Tabarelli, M. (2007) Seed Dispersal by Ants in the Semi-arid Caatinga of North-east Brazil. Annals of Botany, 99: 885-894. doi: 10.1093/aob/mcm017

Leal, L.C., Neto, M.C.L., Oliveira, A.F.M., Andersen, A.N. & Leal, I.R. (2014) Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochorous Euphorbiaceae in Brazilian Caatinga. Oecologia, 174: 493-500. doi: 10.1007/s00442-013-2789-2

Lima, M.H.C., Oliveira, E.G. & Silveira, F.A.O. (2013) Interactions between Ants and Non-myrmecochorous Fruits in Miconia (Melastomataceae) in a Neotropical Savanna. Biotropica, 45: 217-223. doi:10.1111/j.1744-7429.2012.00910.x

Marquitti, F.M.D., Guimarães-Jr, P.R., Pires, M.M. & Bittencourt, L.F. (2013) MODULAR: Software for the Autonomous Computation of Modularity in Large Network Sets. Ecography, 37: 221-224. doi: 10.1111/j.1600-0587.2013.00506.x

Mattos, C.L.V. (2005) Caracterização climática da Restinga da Marambaia. In L.F.T. Menezes, A.L. Peixoto & D.S.D. Araújo (Eds.), História Natural da Marambaia (pp. 55-66). Seropédica: EDUR.

Mello, M.A.R., Marquitti, F.M.D., Guimarães, P.R., Kalko, E.K.V., Jordano, P. & Aguiar, M.A.M. (2011) The modularity of seed dispersal: differences in structure and robustness between bat-and bird-fruit networks. Oecologia, 167: 131-140. doi: 10.1007/s00442-011-1984-2

Mendonza, E. & Dirzo, R. (2007) Seed-size variation determines interspecific differential predation by mammals in a neotropical rain forest. Oikos, 116: 1841-1852. doi: 10.1111/j.0030-1299.2007.15878.x

Menezes, L.F.T. & Araújo, D.S.D. (2005) Formações vegetais da Restinga da Marambaia. In L.F.T. Menezes, A.L. Peixoto & D.S.D. Araújo (Eds.), História Natural da Marambaia (pp. 67-120). Seropédica: EDUR.

Olesen, J.M., Bascompte, J., Dupont, Y.L. & Jordano, P. (2007) The modularity of pollination networks. PNAS, 104: 19891-19896. doi: 10.1073/pnas.0706375104

Palacio, R.D., Valderrama-Ardila, C. & Kattan, G.H. (2016) Generalist Species Have a Central Role In a Highly Diverse Plant-Frugivore Network. Biotropica, 48: 349-355. doi: 10.1111/btp.12290

Passos, L. & Oliveira, P.S. (2002) Ants affect the distribution and performance of seedlings of Clusia criuva, a primarily bird-dispersed rainforest tree. Journal of Ecology, 90: 517-528. doi: 10.1046/j.1365-2745.2002.00687.x

Passos, L. & Oliveira, P.S. (2003) Interactions between ants, fruits and seeds in a restinga forest in south-eastern Brazil. Journal of Tropical Ecology, 19: 261-270. doi: 10.1017/S0266467403003298

Passos, L. & Oliveira, P.S. (2004) Interaction between ants and fruits of Guapira opposita (Nyctaginaceae) in a Brazilian sandy plain rainforest: ant effects on seeds and seedlings. Oecologia, 139: 376-382. doi: 10.1007/s00442-004-1531-5

Pereira, M.G., Menezes, L.F.T. & Schultz, N. (2008) Aporte e decomposição da serapilheira na Floresta Atlântica, Ilha da Marambaia, Mangaratiba, RJ. Ciência Florestal, 18: 443-454. doi: 10.5902/19805098428

Pizo, M.A. & Oliveira, P.S. (1998) Interactions between ants and seeds of a nonmyrmecochorous neotropical tree, Cabralea canjerana (Meliaceae), in the Atlantic forest of southeast Brazil. American Journal of Botany, 85: 669-674. doi: 10.2307/2446536

Pizo, M.A. & Oliveira, P.S. (2000) The use of fruits and seeds by ants in the Atlantic forest of southeast Brazil. Biotropica, 32: 851-861. doi: 10.1111/j.1744-7429.2000.tb00623.x

Pizo, M.A. & Oliveira, P.S. (2001) Size and lipid content of nonmyrmecochorous diaspores: effects on the interaction with litter-foraging ants in the Atlantic rain forest of Brazil. Plant Ecology, 157: 37-52. doi: 10.1023/A:1013735305100.

Plowman, N.S., Hood, A.S.C., Moses, J., Redmond, C., Novotny, V., Klimes, P. & Fayle, T.M. (2017) Network reorganization and breakdown of an ant-plant protection mutualism with elevation. Proceedings of the Royal Society of London B, 284: 20162564. doi: 10.1098/rspb.2016.2564

Rico-Gray, V. & Oliveira, P.S. (2007) The ecology and evolution of ant-plant interactions. Chicago: University of Chicago Press, 331 p

Santana, F.D., Cazetta, E. & Delabie, J.H.C. (2013) Interactions between ants and non¬ myrmecochorous diaspores in a tropical wet forest in southern Bahia, Brazil. Journal of Tropical Ecology, 29: 71-80. doi: 10.1017/S0266467412000715

Silva, B.F., Azevedo, I.H.F., Mayhé-Nunes, A., Breier, T., Nunes-Freitas, A.F. (2019) Ants promote germination of the tree Guarea guidonia by cleaning its seeds. Floresta e Ambiente, 26: e20180151. doi: 10.1590/2179-8087.015118

Silveira, F.A.O., Mafia, P.O., Lemos-Filho, J.P. & Fernandes, G.W. (2012) Species-specific outcomes of avian gut passage on germination of Melastomataceae seeds. Plant Ecology and Evolution, 145: 350-355. doi: 10.5091/plecevo.2012.706

Silvestre, R., Brandão, C.R.F. & Silva, R.R. (2003) Grupos funcionales de hormigas: El caso de los gremios del Cerrado. In F. Fernandez (Ed.), Introducción a las hormigas de la región Neotropical (pp. 101-136). Bogotá: Instituto de Investigación de Recursos Biológicos Alexander von Humboldt.

Van der Pijl, L. (1982) Principles of dispersal in higher plants. Berlin: Springer, 162 p

Watts, S., Dormann, C.F., González, A.M.M. & Ollerton, J. (2016) The influence of floral traits on specialization and modularity of plant–pollinator networks in a biodiversity hotspot in the Peruvian Andes. Annals of Botany, 118: 415-429. doi: 10.1093/aob/mcw114

Wenny, D.G. (2001) Advantages of seed dispersal: A re-evaluation of directed dispersal. Evolutionary Ecology Research, 3: 51-74.

Willott, S.J., Compton, S.G. & Incoll, L.D. (2000) Foraging, food selection and worker size in the seed harvesting ant Messor bouvieri. Oecologia, 125: 35–44. doi: 10.1007/PL00008889

Zwiener, V.P., Bihn, J.H. & Marques, M.C.M. (2012) Ant-diaspore interactions during secondary succession in the Atlantic forest of Brazil. Revista de Biología Tropical, 60: 933–942. doi: 10.15517/rbt.v60i2.4028

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Published

2021-08-14

How to Cite

Laviski, B. F. da S., Mayhé-Nunes, A. J., & Nunes-Freitas, A. F. (2021). Structure of ant-diaspore networks and their functional outcomes in a Brazilian Atlantic Forest. Sociobiology, 68(3), e7104. https://doi.org/10.13102/sociobiology.v68i3.7104

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Research Article - Ants

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