Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-03T02:06:05.818Z Has data issue: false hasContentIssue false
  • English
  • Français

Interactions between ants and non-myrmecochorous diaspores in a tropical wet forest in southern Bahia, Brazil

Published online by Cambridge University Press:  10 January 2013

Flávia Delgado Santana ,
Eliana Cazetta  and
Jacques Hubert Charles Delabie
Flávia Delgado Santana*
Affiliation:
Universidade Estadual de Santa Cruz, Programa de Pós-Graduação Ecologia e Conservação da Biodiversidade, Ilhéus, Bahia Laboratório de Mirmecologia, CEPLAC/CEPEC, Ilhéus, Bahia, Brazil
Eliana Cazetta
Affiliation:
Universidade Estadual de Santa Cruz, Departamento de Ciências Biológicas, Ilhéus, Bahia, Brazil
Jacques Hubert Charles Delabie
Affiliation:
Universidade Estadual de Santa Cruz, Departamento de Ciências Agrárias e Ambientais, Ilhéus, Bahia, Brazil Laboratório de Mirmecologia, CEPLAC/CEPEC, Ilhéus, Bahia, Brazil
*
1Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

Interactions between ants and non-myrmecochorous diaspores occur frequently on the forest floor and the results of these interactions (e.g. diaspore cleaning or removal) will often depend on the morpho-chemical characteristics of the diaspores. We conducted two different experiments with seven plant species in the north-eastern Atlantic forest, Brazil. To evaluate whether ant interactions decrease diaspore persistence time on the forest floor, we established sample stations by placing five diaspores of each species spaced every 10 m along a transect and monitored ant interactions over a 24-h period. We also compared diaspore removal by ants and vertebrates through a paired experiment. We monitored removal of the seven plant species in treatments where ants were excluded and treatments where vertebrates were excluded. We recorded 332 ant–diaspore interactions, most resulting in ants cleaning diaspores in situ. Persistence of diaspores on the forest floor varied greatly among studied species and was less than 50% for three species. Ants also removed more diaspores than did vertebrates. Number of diaspores removed by ants was greater for small diaspores and with high lipid concentration. Ant–diaspore interactions may not always exert a positive influence on plant recruitment for diaspores with poor nutrient concentration. Consequently, ants may play a disproportionately important role as secondary dispersers in tropical forests.

Keywords

ant–diaspore interactionBrazilian Atlantic forestdiaspore persistencefleshy fruitsfrugivoryfruit traitsground-dwelling antssecondary seed dispersalseed cleaningseed removal
Type
Research Article
Information
Journal of Tropical Ecology , Volume 29 , Issue 1 , January 2013 , pp. 71 - 80
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

AMORIM, A. M., THOMAS, W. W. & JARDIM, J. G. 2008. Floristics of the Una Biological Reserve, Bahia, Brazil. Pp. 67–146 in Thomas, W. W. (ed.). The Atlantic coastal forest of northeastern Brazil. New York Botanical Garden Press, New York. 586 pp.Google Scholar
ANDERSEN, A. N., AZCA, F. M. & COWIE, D. 2000. Seed selection by an exceptionally rich community of harvester ants in the Australian seasonal tropics. Journal of Animal Ecology 69:975–984.CrossRefGoogle Scholar
AUGSPURGER, C. K. 1990. Spatial patterns of damping-off disease during seedling recruitment in tropical forests. Pp. 131–144 in Burdon, J. J. & Leather, S. R. (eds.). Pests, pathogens and plant communities. Blackwell Scientific Publications, Oxford. 341 pp.Google Scholar
AUGSPURGER, C. K. & KELLY, C. K. 1984. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61:211–217.CrossRefGoogle ScholarPubMed
BEATTIE, A. J. 1985. The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge. 196 pp.CrossRefGoogle Scholar
BEAUMONT, K. P., MACKAY, D. A. & WHALEN, M. A. 2009. Combining distances of ballistic and myrmecochorous seed dispersal in Adriana quadripartita (Euphorbiaceae). Acta Oecologica 35:429–436.CrossRefGoogle Scholar
BERNSTEIN, R. A. 1975. Foraging strategies of ants in response to variable food density. Ecology 56:213–219.CrossRefGoogle Scholar
BYRNE, M. M. & LEVEY, D. J. 1993. Removal of seeds from frugivore defecations by ants in a Costa Rican rain forest. Plant Ecology 108:363–374.CrossRefGoogle Scholar
CASSANO, C. R., DELABIE, J. H. C., FARIA, D. & BEDE, L. 2009. Landscape and farm scale management to enhance biodiversity conservation in the cocoa producing region of southern Bahia, Brazil. Biodiversity and Conservation 18:577–603.CrossRefGoogle Scholar
CATENACCI, L. S., DE VLEESCHOUWER, K. M. & NOGUEIRA-FILHO, S. L. G. 2009. Seed dispersal by golden-headed lion tamarins Leontopithecus chrysomelas in southern Bahian Atlantic Forest, Brazil. Biotropica 41:744–750.CrossRefGoogle Scholar
CAZETTA, E., SCHAEFER, H. M. & GALETTI, M. 2008. Does attraction to frugivores or defense against pathogens shape fruit pulp composition? Oecologia 155:277–286.CrossRefGoogle ScholarPubMed
CAZETTA, E., GALETTI, M., REZENDE, E. L. & SCHAEFER, H. M. 2012. On the reliability of visual communication in vertebrate-dispersed fruits. Journal of Ecology 100:277–286.CrossRefGoogle Scholar
CHRISTIANINI, A. V. & OLIVEIRA, P. S. 2009. The relevance of ants as seed rescuers of a primarily bird-dispersed tree in the Neotropical cerrado savanna. Oecologia 160:735–745.CrossRefGoogle ScholarPubMed
CHRISTIANINI, A. V. & OLIVEIRA, P. S. 2010. Birds and ants provide complementary seed dispersal in a neotropical savanna. Journal of Ecology 98:573–582.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
CIPOLLINI, M. L. & LEVEY, D. J. 1997. Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. American Naturalist 150:346–372.CrossRefGoogle ScholarPubMed
CRESSWELL, J. E. & OSBORNE, J. L. 2004. The effect of patch size and separation on bumblebee foraging in oilseed rape: implications for gene flow. Journal of Applied Ecology 41:539–546.CrossRefGoogle Scholar
DALLING, J. W., SWAINE, M. D. & GARWOOD, N. C. 1998. Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79:564–578.CrossRefGoogle Scholar
EDWARDS, W., DUNLOP, M. & RODGERSON, L. 2006. The evolution of rewards: seed dispersal, seed size and elaiosome size. Journal of Ecology 94:687–694.CrossRefGoogle Scholar
FARJI-BRENER, A. G. 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.Google Scholar
FOWLER, H. G., FORTI, L. C., BRANDÃO, C. R. F., DELABIE, J. H. C. & VASCONCELOS, H. L. 1991. Ecologia nutricional de formigas. Pp. 131–223 in Panizzi, A. R. & Parra, J. R. P. (eds). Ecologia nutricional de insetos e suas implicações no manejo de pragas. Editora Manole & CNPq, São Paulo. 359 pp.Google Scholar
GORB, S. N. & GORB, E. V. 1999. Dropping rates of elaiosome-bearing seeds during transport by ant, implications for distance dispersal. Acta Oecologica 20:509–518.CrossRefGoogle Scholar
GUIMARÃES, 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.CrossRefGoogle Scholar
HÖLLDOBLER, B. & WILSON, E. O. (eds.). 1990. The ants. Harvard University Press, Cambridge, MA. 746 pp.CrossRefGoogle Scholar
HORVITZ, C. C. 1981. Analysis of how ant behaviour affects germination in a tropical myrmecochore Calathea microcephala (P. & E.) Koernicke (Marantaceae): microsite selection and aril removal by neotropical ants, Odontomachus, Pachycondyla, and Solenopsis (Formicidae). Oecologia 51:47–52.CrossRefGoogle Scholar
HUGHES, L. & WESTOBY, M. 1990. Removal rates of seeds adapted for dispersal by ants. Ecology 71:138–148.CrossRefGoogle Scholar
KASPARI, M. 1996. Worker size and seed size selection by harvester ants in a neotropical forest. Oecologia 105:397–404.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
LEVEY, D. J. & BYRNE, M. M. 1993. Complex ant–plant interactions: rain-forest ants as secondary dispersers and post-dispersal seed predators. Ecology 74:1802–1812.CrossRefGoogle Scholar
MANZANEDA, A. J. & REY, P. J. 2009. Assessing ecological specialization of an ant-seed dispersal mutualism through a wide geographic range. Ecology 90:3009–3022.CrossRefGoogle ScholarPubMed
MANZANEDA, A. J., REY, P. J. & ALCÁNTARA, J. M. 2009. Conflicting selection on diaspore traits limits the evolutionary potential of seed dispersal by ants. Journal of Evolutionary Biology 22:1407–1417.CrossRefGoogle ScholarPubMed
MEHDIABADI, N. & SCHULTZ, T. R. 2010. Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini). Myrmecological News 13:37–55.Google Scholar
MENDOZA, E. & DIRZO, R. 2007. Seed-size variation determines interspecific differential predation by mammals in a neotropical rain forest. Oikos 116:1841–1852.Google Scholar
MILESI, F. A. & CASENAVE, J. L. D. E. 2004. Unexpected relationships and valuable mistakes: non-myrmecochorous Prosopis dispersed by messy leafcutting ants in harvesting their seeds. BioScience 29:558–567.Google Scholar
MORI, S. A. & BOOM, B. M. 1983. Southern Bahian moist forest. Botanical Review 49:155–232.CrossRefGoogle Scholar
NESS, J. H., BRONSTEIN, J. L., ANDERSEN, A. N. & HOLLAND, J. N. 2004. Ant body size predicts dispersal distance of ant-adapted seeds: implications of small-ant invasions. Ecology 85:1244–1250.CrossRefGoogle Scholar
NOGUEIRA, A. R. DE A. & SOUZA, G. B. 2005. Manual de laboratórios: solo, água, nutrição vegetal, nutrição animal e alimentos. (First edition). Embrapa Pecuária Sudeste, São Carlos. 334 pp.Google Scholar
OHKAWARA, K. & AKINO, T. 2004. Seed cleaning behaviour by tropical ants and its anti-fungal effect. Journal of Ethology 23:93–98.CrossRefGoogle Scholar
OLIVEIRA-FILHO, A. T. & FONTES, M. A. L. 2000. Patterns of floristic differentiation among Atlantic Forest in Southeastern Brazil and the influence of climate. Biotropica 32:793–810.CrossRefGoogle Scholar
PASSOS, L. & OLIVEIRA, P. S. 2002. Ants affect the distribution and performance of seedlings of Clusia criuva, a primarily bird-dispersed rain forest tree. Journal of Ecology 90:517–528.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
PFEIFFER, M., NAIS, J. & LINSENMAIR, K. E. 2006. Worker size and seed size selection in ‘seed’-collecting ant ensembles (Hymenoptera: Formicidae) in primary rain forests on Borneo. Journal of Tropical Ecology 22:685–693.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
PIZO, M. A., GUIMARÃES, P. R. & OLIVEIRA, P. S. 2005a. Seed removal by ants from faeces produced by different vertebrate species. Ecoscience 12:136–140.CrossRefGoogle Scholar
PIZO, M. A., PASSOS, L. & OLIVEIRA, P. S. 2005b. Ants as seed disperses of fleshy diaspores in Brazilian Atlantic forests. Pp. 315–329 in Forget, P.M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate. CABI Publishing, Wallingford. 432 pp.Google Scholar
ROBERTS, J. T. & HEITHAUS, E. R. 1986. Ants rearrange the vertebrate-generated seed shadow of a neotropical fig tree. Ecology 67:1046–1051.CrossRefGoogle Scholar
ROWLES, A. D. & O'DOWD, D. J. 2009. New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion. Oecologia 158:709–716.CrossRefGoogle ScholarPubMed
SCHUPP, E. W., JORDANO, P. & GÓMEZ, J. M. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188:333–353.CrossRefGoogle ScholarPubMed
SERVIGNE, P. & DETRAIN, C. 2008. Ant–seed interactions: combined effects of ant and plant species on seed removal patterns. Insectes Sociaux 55:220–230.CrossRefGoogle Scholar
TANG, A. M. C., CORLETT, R. T. & HYDE, K. D. 2005. The persistence of ripe fleshy fruits in the presence and absence of frugivores. Oecologia 142:232–237.CrossRefGoogle ScholarPubMed
THOMAS, W. W., JARDIM, J. G., FIASCHI, P. & AMORIM, A. M. 2003. Lista preliminar das angiospermas localmente endêmicas do sul da Bahia e norte do Espírito Santo, Brasil. Pp. 1–9 in Prado, P. I., Landau, E. C., de Moura, R. T., Pinto, L. P. S., Fonseca, G. A. B. & Alger, K. (eds.). Corredor de biodiversidade da Mata Atlântica do sul da Bahia. IESB/CI/CABS/UFMG/UNICAMP Ilhéus.Google Scholar
VANDER WALL, S. B. & LONGLAND, W. S. 2004. Diplochory: are two seed dispersers better than one? Trends in Ecology and Evolution 19:155–161.CrossRefGoogle ScholarPubMed
VANDER WALL, S. B., KUHN, K. M., BECK, M. J. & ECK, M. A. J. B. 2005. Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806.CrossRefGoogle Scholar
WENNY, D. G. 2001. Advantages of seed dispersal: a re-evaluation of directed dispersal. Evolutionary Ecology Research 3:51–74.Google Scholar
WILBY, A. & SHACHAK, M. 2000. Harvester ant response to spatial and temporal heterogeneity in seed availability: pattern in the process of granivory. Oecologia 125:495–503.CrossRefGoogle ScholarPubMed
ZHOU, H., CHEN, J. & CHEN, F. 2007. Ant-mediated seed dispersal contributes to the local spatial pattern and genetic structure of Globba lancangensis (Zingiberaceae). Journal of Heredity 98:317–324.CrossRefGoogle Scholar