The Habitat Affects the Ecological Interactions between Azteca Forel (Hymenoptera: Formicidae) and Cecropia Loefl. (Urticaceae Juss.)

Marcos Augusto Ferraz Carneiro, André Luiz Gaglioti, Karine Santana Carvalho, Ivan Cardoso Nascimento, Juliana Zina

Abstract


In order to understand the effects of human impacts on structure and functioning of tropical forests, we should consider studies on animal-plant interactions such as antplant mutualistic interactions.We investigated the mutualistic interactions between ants (Azteca genera) and Cecropia plants in habitats of secondary forest and pasture used as cattle fields. We tested for the following hyphothesis: (i) Cecropia from pasture are more susceptible to foliar herbivory than the Cecropia from the forest, and (ii) the defense promoted by ants of Azteca genus is less efficient in the pasture when compared to the forested areas. We selected four areas inserted in Atlantic rain forest domain surrounded by secondary forest and by cattle pastures. The herbivory was more intense in the pasture than in the secondary forest. The presence of Azteca species diminished foliar herbivory only in the forested areas, where we observed a significant increase in herbivory after the removal of A. alfari colony. We argue that the greater herbivory in pasture occurs probably due the lack of other plant resource, being Cecropia paschystachya Trécul and C. glaziovii Snethl., isolated in a “sea of grass” without connection with other tree vegetation, opposite scenario observed in forested habitats. The defense of Azteca only in the secondary forest, leading us to suppose that: 1) not even the your aggressive behavior is able to reduce the intense herbivory in the pasture; 2) the your behavioral pattern in forest is not the same in deforested environments and / or 3) mutualism may be undergoing changes due to abiotic effects on pasture.


Keywords


Mutualism; Atlantic forest; herbivory; ant-plant ecology; conservation

Full Text:

PDF

References


Arnold, A.E. & Asquith, N.M. (2002). Herbivory in a fragmented tropical forest: patterns from islandsat Lago Gatun, Panamá. Biodiversity and Conservation, 11: 1663-1680. doi: 10.1023/A:1016888000369

Barbosa, V.S., Leal, I.R., Iannuzzi, L. & Almeida-Cortez, J. (2005). Distribution pattern of herbivorous insects in a remnant of Brazilian Atlantic forest. Neotropical Entomological, 34: 1-11.doi: 10.1590/S1519-566X2005000500001

Barone, J.A. (1998). Host-specificity of folivorous insects in a moist tropical forest. Journal of Animal Ecology, 67: 400-409. doi: 10.1046/j.1365-2656.1998.00197.x

Basset, Y., Arbelenc, H.P., Barrios, H., Curletti, G., Bérenger, J. M.; Vesco, J. P., Causse, P., Haug, A., Hennion, A.S., Lesobre, L., Marques, F. & O´Meara, R. (2001). Stratification and diel activity of arthropod assemblages. Biological Journal of the Linnean Society, 72: 585-607. doi: 10.1111/j.1095-8312.2001.tb01340.x

Berg, C.C., Rosselli, P.F. & Davidson, D.W. (2005). “Cecropia”. Bronx, New York: Botanical Garden, Flora Neotropica Monograph, 94: 1-230.

Bruna, E.M., Lapola, D.M. & Vasconcelos, H.L. (2004). Interspecific variation in the defensive responses of obligate plant-ants: experimental tests and consequences for herbivory. Oecologia, 138: 558-565. doi: 10.1007/s00442-003-1455-5

Cherrett, J.M. 1986. (1986). The biology, pest status and control of leaf-cutting ants. Agricultural Zoology Reviews, 1: 1-37.

Clavel, J., Julliard, R. & Devictor, V. (2011). Worldwide decline of specialist species: toward a global functional homogenization. Frontiers in Ecology and the Environment 9: 222-228. doi: 10.1890/080216

Coley, P.D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs, 53: 209–233. doi: 10.2307/1942495

Coley, P.D. & Barone, J.A. (2001). Ecology of Defenses. In: S. Levin (ed.). Encyclopedia of Biodiversity (vol.2) (pp.11-21). Amsterdam, The Netherlands: Academic Press.

Coley, P.D. & Barone, J.A. (1996). Herbivory and plant defenses in tropical forest. Annual Review of Ecology and Systematics, 27: 305-335. doi: 10.1146/annurev.ecolsys.27.1.305

Davidson, D.W. (2005). Cecropia and its biotic defenses. In: Berg, C.C. & Rosselli, P.F. Flora Neotropica Monograph 94: Cecropia. New York: Organization for Flora Neotropica, p. 214-226.

Delunardo, F.A.C., Silva, B.F. & Silva, A.G. (2010) Padrões de danos foliares por herbivoria em Ctenanthelanceolata Petersen (Maranthaceae) na Reserva Biológica de Duas Bocas, Cariacica, Espírito Santo. Natureza on line, 8 (2): 95-97. Retrived from: http://www.naturezaonline.com.br

Fahrig, L. (2013). Rethinking patch size and isolation effects: the habitat amount hypothesis. Journal of Biogeography 40:1649–1663. doi: 10.1111/jbi.12130

Fáveri, S.B. & Vasconcelos, H.L. (2004). The Azteca-Cecropia association: are ants always necessary for their host plants? Biotropica, 36: 641-646. doi: 10.1111/j.1744-7429.2004.tb00359.x

Frederickson, M.E. (2005). Ant species confer different partner benefits on two Neotropical myrmecophytes. Oecologia, 143: 387-395. doi: 10.1007/s00442-004-1817-7

Geist, H.J. & Lambin, E.F. (2002). Proximate causes and underlying driving forces of tropical deforestation. Bioscience, 52: 143-150. doi: 10.1641/0006-3568(2002)052[0143:PCAUDF]2.0.CO;2

Guimarães, C.D.D., Viana, J.P.R. & Cornelissen, T. (2014). A meta-analysis of the effects of fragmentation on herbivorous insects. Environmental Entomology, 43: 537-545. doi: 10.1603/EN13190

Harada, A.Y. & Benson, W.W. (1988). Espécies deAzteca (Hymenoptera, Formicidae) especializadas em Cecropia spp. (Moraceae): distribuição geográfica e considerações ecológicas. Revista Brasileira de Entomologia, 32: 423-435.

Heil, M. & D. Mckey. (2003). Protective ant-plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology, Evolution, and Systematics, 34: 425-453. doi: 10.1146/annurev.ecolsys.34.011802.132410

Hunter, M.D., Ohgushi, T. & Price, P.W. (1992). Effects of resource distribution on animal-plant interactions. Academic Press, San Diego. doi: 10.2307/3809408

Izzo, T. & Vasconcelos, H.L. (2002). Cheating the cheater: Domatia loss minimizes the effects of ant castration in an Amazonian ant-plant. Oecologia, 133: 200-205. doi: 10.1007/s00442-002-1027-0

Janzen, D.H. (1969). Allelopathy by myrmecophytes: the ant Azteca as an allelopathic agent of Cecropia. Ecology, 50: 147-153. doi: 10.2307/1934677

Jolivet, P. (1990). Relative protection of Cecropia trees against leaf-cutting ants in tropical America. In: Meer, R.K.V., Jaffe, K. & Cedeno, A. (eds.). Applied Myrmecology: A World Perspective. (pp.251-254). San Francisco: Westview Press.

Kim, T.N. (2017). How plant neighborhood composition influences herbivory: Testing four mechanisms of associational resistance and susceptibility. PLoS ONE, 12: e0176499. doi: 10.1371/journal.pone.0176499

Laurance, W.F., Nascimento, H.E.M., Laurance, S.G., Andrade, A., Ewers, R.M., Harms, K.E., Luizão, R.C.C. & Ribeiro, J.E. (2007). Habitat fragmentation, variable edge effects, and the landscape-divergence hypothesis. PLoS ONE, 2: e1017. doi: 10.1371/journal.pone.0001017

Laurance, W.F., Nascimento, H.E.M., Laurance, S.G., Andrade, A., Ribeiro, J.E. & Giraldo, J.P. (2006). Rapid decay of tree-community composition in Amazonian forest fragments. Proceedings of the National Academy of Sciences USA, 103: 19010-19014. doi: 10.1073/pnas.0609048103

Letourneau, D.K., Armbrecht, I., Rivera, B.S., Lerma, J.M., Carmona, E.J., Daza, M.C., Escobar, S., Galindo, V., Gutiérrez, C., Lópes, S.D., Mejía, J.L., Rangel, A.M.A., Rangel, J.H., Rivera, L., Saavedra, C. A., Torres, A. M. & Trujillo, A.R. (2011). Does plant diversity benefit agroecosystems? A synthetic review. Ecological Applications, 21: 9-21. doi: 10.1890/09-2026.1

Llandres, A.L., Rodriguez-Girones, M.A. & Dirzo, R. (2011). Plant stages with biotic, indirect defences are more palatable and suffer less herbivory than their undefended counterparts. Biological Journal of the Linnean Society, 101: 536-543. doi: 10.1111/j.1095-8312.2010.01521.x

Lôbo, D., Leão, T., Melo, F.P.L., Santos, A.M.M. & Tabarelli, M. (2011). Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Diversity and Distributions, 17: 287-296. doi: 10.1111/j.1472-4642.2010. 00739.x

Longino, J.T. (2005). The Cecropia-Azteca Association in Costa Rica. . Acesso em: 01/02/2017.

Longino, J.T. (1991). Azteca ants in Cecropia trees: taxonomy, colony structure, and behavior. In: Huxley, C.R. & Cuttler, D.F. Ant-plant Interactions. (pp. 271-288). New York: Oxford Science Publications.

Longino, J.T. (1989). Geographic variation and community structure in an ant-plant mutualism: Azteca and Cecropia in Costa Rica. Biotropica, 21: 126-132. doi:10.2307/2388703

Morante-Filho, J.C., Arroyo-Rodríguez, V., Lohbeck, M., Tscharntke, T. & Faria, D. (2016). Tropical forest loss and its multitrophic effects on insect herbivory. Ecology, 97: 3315-3325: doi: 10.1002/ecy.1592

Murcia, C. (1995). Edge effects in fragmented forests: implications for conservation. Trends in Ecology and Evolution, 10: 58-62. doi: 10.1016/S0169-5347(00)88977-6

Neves, F.S., Sperber, C.F., Campos, R.I., Soares, J.P. & Ribeiro, S.P. (2013). Contrasting effects of sampling scale on insect herbivores distribution in response to canopy structure. Revista de Biologia Tropical, 61: 125-137.ISSN 0034-7744

Ohata, M., Furumoto, A. & Ohsaki, N. (2010). Local adaptations of larvae of the butterfly Pierisnapi to physical and physiological traits of two Arabis plants (Cruciferae). Ecological Research, 25: 33-39. doi: 10.1007/s11284-009-0625-2

Pacheco, P.S.M. Jr. & Del-Claro, K. (2015). Nestmate Recognition in the Amazonian Myrmecophyte Ant Pseudomyrmex concolor Smith (Hymenoptera: Formicidae). Sociobiology 62: 356-363. doi: 10.13102/sociobiology.v62i3.746

Peter, F., Berens, D.G., Grieve, G.R. & N. Farwig. (2015). Forest fragmentation drives the loss of insectivorous birds and an associated increase in herbivory. Biotropica, 47: 626-635. doi: 10.1111/btp.12239

Power, M.E. (1992). Top-down and bottom-up forces in food webs: Do plants have primacy? Ecology 73: 733- 746. doi: 10.2307/1940153

Rao, M. (2000). Variation in leaf-cutter ant (Atta sp.) densities in forest isolates: the potential role of predation. Journal of Tropical Ecology, 16: 209-225. doi: 10.1017/S026646740000136X

Rosumek, F.B., Silveira, F.A.O., Neves, F.D.S., Barbosa, N.P.D.U., Diniz, L., Oki, Y., Pezzini, F., Fernandes, G. W. & Cornelissen, T. (2009). Ants on plants: A meta-analysis of the role of ants as plant biotic defenses. Oecologia, 160: 537-549. doi: 10.1007/s00442-009-1309-x

Sanchez-Azofeifa, G.A. & Portillo-Quintero, C. (2011). Extent and Drivers of Change of Neotropical Dry Forest. In:Dirzo, R., Mooney, H. & Ceballos, G. (Eds). Seasonally Dry Tropical Forests. (pp. 45-57). Stanford University Centre for Latin American Studies and Universidad Autonomy de Mexico. Standford University Press.

Shahabuddin, G. & Terborgh, J.W. (1999). Frugivorous butterflies in Venezuelan forest fragments: abundance, diversity, and the effects of isolation. Journal of Tropical Ecology, 15: 703-722. doi: 10.1017/S0266467499001121

Sposito, T.C.S. & Santos, F.A.M. (2001). Architectural patterns of eight Cecropia (Cecropiaceae) species of Brazil. Flora, 196: 215-226. doi: 10.1016/S0367-2530(17)30043-9

SYSTAT. (2007). Systat Software (data analysis software system), version 12.0. San Jose, CA. www.systatsoftware.com

Tabarelli, M., Peres, C.A. & Melo, F.P.L. (2012). The ‘few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biological Conservation, 155: 136-140.

Tahvanainen J.O. & Root R.B. (1972). The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia, 10: 321-46. doi: 10.1007/BF00345736 PMID: 28307065 2

Terborgh J., Lopez L., Tello, J., Yu, D. & Bruni, A.R. (1997). Transitory states in relaxing ecosystems of land-bridge islands. In: Laurance W.F. & Bierregaard R.O. Jr. Tropical Forest Remnants: Ecology, Management, and Conservation of Fragmented Communities, pp. 256–274. University of Chicago Press, Chicago.

Urbas, P., Araujo Jr, M.V., Leal, I.R. & Wirth, R. (2007). Cutting More from Cut Forest: Edge Effects on Foraging and Herbivory of Leaf-Cutting Ants in Brazil. Biotropica, 39: 489-495. doi: 10.1111/j.1744-7429.2007.00285.x

Vasconcelos, H.L. & Casimiro, A.B. (1997). Influence of Azteca alfari ants on the exploitation of Cecropia trees by a leaf-cutting ant. Biotropica, 29: 84-92. doi: 10.1111/j.1744-7429.1997.tb00009.x

Yamamoto, M. & Del-Claro, K. (2008). Natural history and foraging behavior of the carpenter ant Camponotus sericeiventris Guérin, 1838 (Formicinae, Campotonini) in the Brazilian tropical savanna. Acta Ethologica, 11: 55-65. 2008. doi: 10.1007/s10211-008-0041-6

Yu, D.W. & Davidson, D.W. (1997). Experimental studies of species-specificity in Cecropia–ant relationships. Ecological Monographs, 67: 273-294. doi: 10.1890/0012- 9615(1997) 067[0273:ESOSSI]2.0.CO;2

Zar, J. H. (1996). Biostatiscal Analysis. Third edition. Prentice Hall. Upper Saddle River, NJ, USA. 662p.




DOI: http://dx.doi.org/10.13102/sociobiology.v65i2.2044

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2018: 0.604