Ant-caterpillar Antagonism At The Community Level: Interhabitat Variation Of Tritrophic Interactions In A Neotropical Savanna

Ant foraging on foliage can substantially affect how phytophagous insects use host plants and represents a high predation risk for caterpillars, which are important folivores. Ant-plant-herbivore interactions are especially pervasive in cerrado savanna due to continuous ant visitation to liquid food sources on foliage (extrafloral nectaries, insect honeydew). While searching for liquid rewards on plants, aggressive ants frequently attack or kill insect herbivores, decreasing their numbers. Because ants vary in diet and aggressiveness, their effect on herbivores also varies. Additionally, the differential occurrence of ant attractants (plant and insect exudates) on foliage produces variable levels of ant foraging within local floras and among localities. Here, we investigate how variation of ant communities and of traits among host plant species (presence or absence of ant attractants) can change the effect of carnivores (predatory ants) on herbivore communities (caterpillars) in a cerrado savanna landscape. We sampled caterpillars and foliage-foraging ants in four cerrado localities (70-460 km apart). We found that: (i) caterpillar infestation was negatively related with ant visitation to plants; (ii) this relationship depended on local ant abundance and species composition, and on local preference by ants for plants with liquid attractants; (iii) this was not related to local plant richness or plant size; (iv) the relationship between the presence of ant attractants and caterpillar abundance varied among sites from negative to neutral; and (v) caterpillars feeding on plants with ant attractants are more resistant to ant predation than those feeding on plants lacking attractants. Liquid food on foliage mediates host plant quality for lepidopterans by promoting generalized ant-caterpillar antagonism. Our study in cerrado shows that the negative effects of generalist predatory ants on herbivores are detectable at a community level, affecting patterns of abundance and host plant use by lepidopterans. The magnitude of ant-induced effects on caterpillar occurrence across the cerrado landscape may depend on how ants use plants locally and how they respond to liquid food on plants at different habitats. This study enhances the relevance of plant-ant and ant-herbivore interactions in cerrado and highlights the importance of a tritrophic perspective in this ant-rich environment. Ants are major predators of insect herbivores in tropical habitats. In the Brazilian savanna, negative effects by predatory ants on herbivores (caterpillars) are detectable at the community level, affecting patterns of host plant use by lepidopteran communities. The study highlights the importance of a tritrophic perspective in this ant-rich environment.842442452Anderson, M.J., A new method for non-parametric multivariate analysis of variance (2001) Austral Ecology, 26, pp. 32-46Barton, A.M., Spatial variation in the effect of ants on an extrafloral nectary plant (1986) Ecology, 67, pp. 495-504Bernays, E.A., Evolution of feeding behavior in insect herbivores: success seen as different ways to eat without being eaten (1998) BioScience, 48, pp. 35-44Blüthgen, N., Gebauer, G., Fiedler, K., Disentangling a rainforest food web using stable isotopes: dietary diversity in a species-rich ant community (2003) Oecologia, 137, pp. 426-435Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H., Generalized linear mixed models: a practical guide for ecology and evolution (2009) Trends in Ecology and Evolution, 24, pp. 127-135Bronstein, J.L., Our current understanding of mutualism (1994) Quarterly Review of Biology, 69, pp. 31-51Bronstein, J.L., The contribution of ant-plant protection studies to our understanding of mutualism (1998) Biotropica, 30, pp. 150-161Brown, K.S., Gifford, D.R., Lepidoptera in the cerrado landscape and the conservation of vegetation, soil, and topographical mosaics (2002) The Cerrados of Brazil, pp. 201-222. , eds P.S. Oliveira & R.J. Marquis) -. Columbia University Press, New YorkByk, J., Del-Claro, K., Nectar- and pollen-gathering Cephalotes ants provide no protection against herbivory: a new manipulative experiment to test ant protective capabilities (2010) Acta Ethologica, 13, pp. 33-38Chamberlain, S.A., Holland, J.N., Density-mediated, context-dependent consumer-resource interactions between ants and extrafloral nectar plants (2008) Ecology, 89, pp. 1364-1374Davidson, D.W., Cook, S.C., Snelling, R.R., Chua, T.H., Explaining the abundance of ants in lowland tropical rainforest canopies (2003) Science, 300, pp. 969-972Del-Claro, K., Oliveira, P.S., Ant-Homoptera interactions in a neotropical savanna: the honeydew-producing treehopper, Guayaquila xiphias (Membracidae), and its associated ant fauna on Didymopanax vinosum (Araliaceae) (1999) Biotropica, 31, pp. 135-144De-Silva, D.L., Vásquez, A.S., Mallet, J., Selection for enemy-free space: eggs placed away from the host plant increase survival of a neotropical ithomiine butterfly (2011) Ecological Entomology, 36, pp. 667-672Díaz-Castelazo, C., Rico-Gray, V., Oliveira, P.S., Cuautle, M., Extrafloral nectary-mediated ant-plant interactions in the coastal vegetation of Veracruz, Mexico: richness, occurrence, seasonality and ant foraging patterns (2004) Ecoscience, 11, pp. 472-481Diniz, I., Morais, H.C., Lepidopteran caterpillar fauna of cerrado host plants (1997) Biodiversity and Conservation, 6, pp. 817-836Diniz, I., Braga, L., Lepesqueur, C., Silva, N., Morais, H., (2013) Lagartas do Cerrado - Guia de Campo, , Technical Books, Rio de JaneiroDutra, H.P., Freitas, A.V.L., Oliveira, P.S., Dual ant attraction in the neotropical shrub Urera baccifera (Urticaceae): the role of ant visitation to pearl bodies and fruits in herbivore deterrence and leaf longevity (2006) Functional Ecology, 20, pp. 252-260Dyer, L.A., Effectiveness of caterpillar defenses against three species of invertebrate predators (1997) Journal of Research on Lepidoptera, 34, pp. 48-68Floren, A., Biun, A., Linsenmair, K.E., Arboreal ants as key predators in tropical lowland rainforest trees (2002) Oecologia, 131, pp. 137-144Freitas, A.V.L., Oliveira, P.S., Biology and behavior of Eunica bechina (Lepidoptera: Nymphalidae) with special reference to larval defense against ant predation (1992) Journal of Research on Lepidoptera, 31, pp. 1-11Freitas, A.V.L., Oliveira, P.S., Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly (1996) Journal of Animal Ecology, 65, pp. 205-210Gentry, G.L., Dyer, L.A., On the conditional nature of neotropical caterpillar defenses against their natural enemies (2002) Ecology, 83, pp. 3108-3119Hammer, Ø., Harper, D.A.T., Ryan, P.D., PAST: Paleontological statistics software package for education and data analysis (2001) Palaeontologia Electronica, 4, p. 9. , http://palaeo-electronica.org/2001_1/past/issue1_01.htmHeil, M., McKey, D., Protective ant-plant interactions as model systems in ecological and evolutionary research (2003) Annual Review of Ecology Evolution and Systematics, 34, pp. 425-453Heil, M., Fiala, B., Baumann, B., Linsenmair, K.E., Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius (2000) Functional Ecology, 14, pp. 749-757Hölldobler, B., Wilson, E.O., (1990) The Ants, , Belknap Press, Cambridge, MA(2012), http://www.inmet.gov.br/html/clima.php#, ClimaJeanne, R.L., A latitudinal gradient in rates of ant predation (1979) Ecology, 60, pp. 1211-1224Kaminski, L.A., Freitas, A.V.L., Oliveira, P.S., Interaction between mutualisms: ant-tended butterflies exploit enemy-free space provided by ant-treehopper associations (2010) American Naturalist, 176, pp. 322-334Koptur, S., Experimental evidence for defense of Inga (Mimosoideae) saplings by ants (1984) Ecology, 65, pp. 1787-1793Letourneau, D.K., Passive aggression: an alternative hypothesis for the Piper-Pheidole association (1983) Oecologia, 60, pp. 122-126Letourneau, D.K., Dyer, L.A., Multi-trophic interactions and biodiversity: beetles, ants, caterpillars, and plants (2005) Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity, pp. 366-385. , eds D.F.R.P. Burslem, M.A. Pinard & S.E. Hartley) -. Cambridge University Press, CambridgeLetourneau, D.K., Dyer, L.A., Vega, G.C., Indirect effects of a top predator on a rain forest understory plant community (2004) Ecology, 85, pp. 2144-2152Lill, J.T., Marquis, R.J., The effects of leaf quality on herbivore performance and attack from natural enemies (2001) Oecologia, 126, pp. 418-428Machado, G., Freitas, A.V.L., Larval defence against ant predation in the butterfly Smyrna blomfildia (2001) Ecological Entomology, 26, pp. 436-439Machado, S.R., Morellato, L.P.C., Sajo, M.J., Oliveira, P.S., Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian cerrado (2008) Plant Biology, 10, pp. 660-673Magurran, A.E., (2004) Measuring Biological Diversity, , Wiley-Blackwell, OxfordMody, K., Linsenmair, K.E., Plant-attracted ants affect arthropod community structure but not necessarily herbivory (2004) Ecological Entomology, 29, pp. 217-225Mooney, K.A., Pratt, R.T., Singer, M.S., The tri-trophic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores (2012) PLoS One, 7, p. e34403Oliveira, P.S., The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae) (1997) Functional Ecology, 11, pp. 323-330Oliveira, P.S., Brandão, C.R.F., The ant community associated with extrafloral nectaries in the Brazilian cerrados (1991) Ant-Plant Interactions, pp. 198-212. , eds C.R. Huxley & D.F. Cutler) -. Oxford University Press, OxfordOliveira, P.S., Freitas, A.V.L., Ant-plant-herbivore interactions in the neotropical cerrado savanna (2004) Naturwissenschaften, 91, pp. 557-570Oliveira, P.S., Leitão-Filho, H.F., Extrafloral nectaries: their taxonomic distribution and abundance in the woody flora of cerrado vegetation in southeast Brazil (1987) Biotropica, 19, pp. 140-148Oliveira, P.S., Oliveira-Filho, A.T., Distribution of extrafloral nectaries in the woody flora of tropical communities in Western Brazil (1991) Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, pp. 163-175. , eds P.W. Price, T.M. Lewinsohn, G.W. Fernandes & W.W. Benson)-. John Wiley & Sons, New YorkOliveira-Filho, A.T., Ratter, J.A., Vegetation physiognomies and woody flora of the cerrado biome (2002) The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna, pp. 91-120. , eds P.S. Oliveira & R.J. Marquis) -. Columbia University Press, New YorkPemberton, R.W., Lee, J.H., The influence of extrafloral nectaries on parasitism of an insect herbivore (1996) American Journal of Botany, 83, pp. 1187-1194Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N., Weis, A.E., Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies (1980) Annual Review of Ecology and Systematics, 11, pp. 41-65(2012) R: A Language and Environment for Statistical Computing, , R Foundation for Statistical Computing, Vienna, AustriaRibas, C.R., Schoereder, J.H., Pic, M., Soares, S.M., Tree heterogeneity, resource availability, and larger scale processes regulating arboreal ant species richness (2003) Austral Ecology, 28, pp. 305-314Rico-Gray, V., Oliveira, P.S., (2007) The Ecology and Evolution of Ant-Plant Interactions, , University of Chicago Press, ChicagoRudgers, J.A., Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism (2004) Ecology, 85, pp. 192-205Schmitz, O.J., Krivan, V., Ovadia, O., Trophic cascades: the primacy of trait-mediated indirect interactions (2004) Ecology Letters, 7, pp. 153-163Schoereder, J.H., Sobrinho, T.G., Madureira, M.S., Ribas, C.R., Oliveira, P.S., The arboreal ant community visiting extrafloral nectaries in the Neotropical cerrado savanna (2010) Terrestrial Arthropod Reviews, 3, pp. 3-27Sendoya, S.F., Freitas, A.V.L., Oliveira, P.S., Egg-laying butterflies distinguish predaceous ants by sight (2009) American Naturalist, 174, pp. 134-140Sendoya, S.F., Oliveira, P.S., Data from: Ant-caterpillar antagonism at the community level: interhabitat variation of tritrophic interactions in a neotropical savannah (2014) Dryad Digital RepositorySinger, M.S., Farkas, T.E., Skorik, C.M., Mooney, K.A., Tritrophic interactions at a community level: effects of host plant species quality on bird predation of caterpillars (2012) American Naturalist, 179, pp. 363-374Smiley, J.T., Heliconius caterpillar mortality during establishment on plants with and without attending ants (1985) Ecology, 66, pp. 845-849Styrsky, J.D., Eubanks, M.D., Ecological consequences of interactions between ants and honeydew-producing insects (2007) Proceedings of the Royal Society B, Biological Sciences, 274, pp. 151-164Thompson, J.N., (2005) The Geographic Mosaic of Coevolution, , The University of Chicago Press, ChicagoThompson, J.N., Pellmyr, O., Evolution of oviposition behavior and host preference in Lepidoptera (1991) Annual Review of Entomology, 36, pp. 65-89Tillberg, C.V., Friend or foe? A behavioral and stable isotopic investigation of an ant-plant symbiosis (2004) Oecologia, 140, pp. 506-515Tobin, J.E., Ecology and diversity of tropical forest canopy ants (1995) Forest Canopies, pp. 129-147. , eds M.D. Lowman & N.M. Nadkarni) -. Academic Press, New York(2002) Multitrophic Level Interactions, , Tscharntke, T. & Hawkins, B.A. (eds) () . Cambridge University Press, CambridgeZuur, A.F., Ieno, E.N., Walker, N., Saveliev, A.A., Smith, G.M., (2009) Mixed Effects Models and Extensions in Ecology with R, , Springer, Dordrech

Does Inundation Risk Affect Leaf-cutting Ant Distribution? A Study Along A Topographic Gradient Of A Costa Rican Tropical Wet Forest

Abstract: Successional state of forest and availability of pioneer plants are recognized factors affecting densities of leaf-cutting ants. However little is known about how abiotic factors can shape nest distributions. We investigated the effect of topography, soil, forest successional state and inundation risk on nest density and size of Atta cephalotes colonies along streams in a tropical wet forest in Costa Rica. In each forest type, we surveyed 12 sites, each site comprising five transects (10 × 100 m) varying in topography and proximity to streambeds. We found no difference regarding nest size or density between forest types or soil consociation. Nest density varied with topographic environment, with significantly higher nest density on slope tops (farther from streambeds) and without colonies in valley bottoms (closer to streambeds). Nests found in areas affected by the last great inundation before our study were scarcer and smaller than nests in non-flooded areas. We showed that inundation events favour an accumulation of Atta colonies towards higher sites, where they are also allowed to become larger and may survive longer. Inundation risk may be a strong force shaping the distribution of leaf-cutting ant nests in tropical floodplain forests, even concealing the relevance of successional state of forest. Copyright © Cambridge University Press 2013.3018992Adis, J., Eco-entomological observations from the Amazon: III. How do leaf-cutting ants of inundation forest survive flooding? (1982) Acta Amazonica, 12, pp. 839-840Bitancourt, A.A., Expressao mateḿatica do crescimento de formigueiros de Atta sexdens rubropilosa representado pelo aumento do ńumero de olheiros (1941) Arquivos Do Instituto Bioĺogico de Sao Paulo, 12, pp. 229-237Corella, O., (2001) Elaboracíon de un Mapa Hist́orico Del Cambio de Uso Del Suelo en la Estacíon Bioĺogica la Selva, PuertoViejo de Sarapiqú?, Heredia, , Doctoral thesis, Instituto Tecnoĺogico de Costa RicaCosarinsky, M.I., Roces, F., Neighbor leaf-cutting ants and mound-building termites: Comparative nest micromorphology (2007) Geoderma, 141 (3-4), pp. 224-234. , DOI 10.1016/j.geoderma.2007.06.006, PII S0016706107001644Denslow, J.S., Tropical rainforest gaps and tree species diversity (1987) Annual Review of Ecology and Systematics, 18, pp. 431-451Farji-Brener, A.G., Why are leaf-cutting ants more common in early secondary forests than in old-growth tropical forests? An evaluation of the palatable forage hypothesis (2001) Oikos, 92 (1), pp. 169-177(2006) World Reference Base for Soil Resources. World Soil Resources Reports, (103), 128p. , IUSS WORKING GROUP WRB FAO, RomeKleineidam, C., Roces, F., Carbon dioxide concentrations and nest ventilation in nests of the leaf-cutting ant Atta vollenweideri (2000) Insectes Sociaux, 47, pp. 241-248Laurance, W.F., Ferreira, L.V., Rankin-de Merona, J.M., Laurance, S.G., Rain forest fragmentation and the dynamics of Amazonian tree communities (1998) Ecology, 79 (6), pp. 2032-2040McDade, L.A., Bawa, K.S., Hespenheide, H.A., Hartshorn, G.S., (1994) La Selva: Ecology and Natural History of A Neotropical Rain Forest, 493p. , University of Chicago Press, ChicagoPenaloza, C., Farji-Brener, A.G., The importance of treefall gaps as foraging sites for leaf-cutting ants depends on forest age (2003) Journal of Tropical Ecology, 19 (5), pp. 603-605. , DOI 10.1017/S0266467403003675Schnitzer, S.A., Carson, W.P., Treefall gaps and the maintenance of species diversity in a tropical forest (2001) Ecology, 82 (4), pp. 913-919Silva, P.S.D., Bieber, A.G.D., Leal, R., Wirth, I.R., Tabarelli, M., Decreasing abundance of leaf-cutting ants across a chronosequence of advancing Atlantic forest regeneration (2009) Journal of Tropical Ecology, 25, pp. 223-227Sokal, R.R., Rohlf, F.J., (1995) Biometry: The Principles and Practice of Statistics in Biological Research, p. 887. , (Third edition W. H. Freeman and Co., New YorkSollins, P., Sancho, F.M., Mata, R.C., Sanford, R., Soils and soil process research (1994) La Selva: Ecology and Natural History of A Neotropical Rain Forest, pp. 34-53. , McDade, L. A., Bawa, K. S., Hespenheide, H. A. & Hartshorn, G. S. (eds. University of Chicago Press, ChicagoVan Gils, H.A.J.A., Gaigl, A., Ǵomez, L.E., The relationship between soil variables and leafcutter ant (Atta sexdens) nest distribution in the Colombian Amazon (2010) Insectes Sociaux, 57, pp. 487-49

Behavioral Ecology At The Ant-plant-herbivore Interface: Interactions Between Ants And Lepidopterans [ecologia Comportamental Na Interface Formiga-planta-herbívoro: Interações Entre Formigas E Lepidópteros]

Ants are one of the most prominent groups of terrestrial organisms in terms of diversity, relative abundance, and biomass. Their importance is due primarily to eusociality combined with complex communication systems, which enable them to recruit nestmates to capture prey and/or protect profitable resources. Tropical foliage is rich in renewable food sources that promote visitation by ants. Because they are the principle predators among foliage, ants can strongly affect the communities of herbivorous insects and promote trophic cascades with relevant consequences to plants. The presence of ants on foliage can affect herbivores in two ways: (1) ant foragers can decrease the number of herbivores on plants through antagonistic interactions (e.g. aggressiveness, predation), (2) ants can create an enemy-free space for myrmecophilous herbivores (i.e. those living in close association with ants). Here, we discuss the ecological scenario in which these interactions occur, and examine the effects of foliage-dwelling ants on the biology and behavior of lepidopteran larvae.1312744Adlung, K.G., A critical evaluation of the European research on use of Red Wood ants (Formica rufa group) for the protection of forests against harmful insects (1966) Zeitschrift Fuer Angewandte Entomologie, 57, pp. 167-189Agrawal, A.A., Rutter, M.T., Dynamic anti-herbivore defense in ant-plants: The role of induced responses (1998) Oikos, 83, pp. 227-236Akino, T., Knapp, J.J., Thomas, J.A., Elmes, G.W., Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies (1999) Proceedings of The Royal Society of London B, 266, pp. 1419-1426Als, T.D., Vila, R., Kandul, N.P., Nash, D.R., Yen, S.-H., Hsu, Y.-F., Mignault, A.A., Pierce, N.E., The evolution of alternative parasitic life histories in large blue butterflies (2004) Nature, 432, pp. 386-390Ando, Y., Ohgushi, T., Ant- and plant-mediated indirect effects induced by aphid colonization on herbivorous insects on tall goldenrod (2008) Population Ecology, 50, pp. 181-189Araújo, L.M., Lara, A.C.F., Fernandes, G.W., Utilization of Apion sp. (Coleoptera: Apionidae) galls by an ant community in southeast Brazil (1995) Tropical Zoology, 8, pp. 319-324Atsatt, P.R., Lycaenidae butterflies and ants: Selection for enemy-free space (1981) American Naturalist, 118, pp. 638-654Atsatt, P.R., Ant-dependent food plant-selection by the mistletoe butterfly Ogyris am aryllis (Lycaenidae) (1981) Oecologia, 48, pp. 60-63Axén, A.H., Leimar, O., Hoffman, V., Signalling in a mutualistic interaction (1996) Animal Behaviour, 52, pp. 321-333Barton, A.M., Spatial variation in the effect of ants on an extrafloral nectary plant (1986) Ecology, 67, pp. 495-504Beattie, A.J., (1985) The Evolutionary Ecology of Ant-plant Mutualisms, p. 204. , Cambridge University Press, CambridgeBeattie, A.J., Hughes, L., Ant-plant interactions (2002) C.m. Herrera & O. Pellmyr, pp. 211-135. , (eds.). Plant animal Interactions. Blackwell Publishing, OxfordBernays, E., Graham, M., On the evolution of host specificity in phytophagous arthropods (1988) Ecology, 69, pp. 886-892Bernays, E.A., Feeding by lepidopteran larvae is dangerous (1997) Ecological Entomology, 22, pp. 121-123Bernays, E.A., Cornelius, M.L., Generalist caterpillar prey are more palatable than specialists for the generalist predator Iridomyrmex humilis (1989) Oecologia, 79, pp. 427-430Bluthgen, N., Reifenrath, K., Extrafloral nectaries in an Australian rainforest: Structure and distribution (2003) Australian Journal of Botany, 51, pp. 515-527Bronstein, J.L., Our current understanding of mutualism (1994) Quarterly Review of Biology, 69, pp. 31-51Buckley, R.C., Interactions involving plants, homoptera, and ants (1987) Annual Review of Ecology and Systematics, 18, pp. 111-135Campbell, D.L., Pierce, N.E., Phylogenetic relationships of the Riodinidae: Implications for the evolution of ant association (2003) Butterflies: Ecology and Evolution Taking Flight, pp. 395-408. , In: C.L. Boggs, W.B. Watt & P.R. Ehrlich (eds.), University of Chicago, Chicago. 784pCaveney, S., McLean, H., Surry, D., Faecal firing in a skipper caterpillar is pressure-driven (1998) Journal of Experimental Biology, 201, pp. 121-133Coley, P.D., Barone, J.A., Herbivory and plant defenses in tropical forests (1996) Annual Review of Ecology and Systematics, 27, pp. 305-335Coley, P.D., Bateman, M.L., Kursar, T.A., The effects of plant quality on caterpillar growth and defense against natural enemies (2006) Oikos, 115, pp. 219-228Cottrell, C.B., Aphytophagy in butterflies: Its relationship to myrmecophily (1984) Zoological Journal of Linnean Society, 79, pp. 1-57Daniels, H., Gottsberger, G., Fiedler, K., Nutrient composition of larval nectar secretions from three species of myrmecophilous butterflies (2005) Journal of Chemical Ecology, 31, pp. 2805-2821Davidson, D.W., The role of resource imbalances in the evolutionary ecology of tropical arboreal ants (1997) Biological Journal of The Linnean Society, 61, pp. 153-181Davidson, D.W., Cook, S.C., Snelling, R.R., Chua, T.H., Explaining the abundance of ants in lowland tropical rainforest canopies (2003) Science, 300, pp. 969-972Dejean, A., McKey, D., Gibernau, M., Belin, M., The arboreal ant mosaic in a Cameroonian rainforest (Hymenoptera: Formicidae) (2000) Sociobiology, 35, pp. 403-423Del-Claro, K., Oliveira, P.S., Ant-Homoptera interactions in a neotropical savanna: The honeydew-producing treehopper, Guayaquila xiphias (Membracidae), and its associated ant fauna on Didymopanax vinosum (Araliaceae) (1999) Biotropica, 31, pp. 135-144Devries, P.J., The larval ant-organs of thisbe irenea (Lepidoptera: Riodinidae) and their effects upon attending ants (1988) Zoological Journal of Linnean Society, 94, pp. 379-393Devries, P.J., Enhancement of symbioses between butterfly caterpillars and ants by vibrational communication (1990) Science, 248, pp. 1104-1106Devries, P.J., Evolutionary and ecological patterns in myrmecophilous riodinid butterflies (1991) Ant-plant Interactions, pp. 143-156. , In: C. R. Huxley, & D.F. Cutler (eds.), Oxford University Press, OxfordDevries, P.J., Mutualism between thisbe irenea butterflies and ants, and the role of ant ecology in the evolution of larval-ant associations (1991) Biological Journal of Linnean Society, 43, pp. 179-195Devries, P.J., Call production by myrmecophilous riodinid and lycaenid butterfly caterpillars (Lepidoptera): Morphological, acoustical, functional, and evolutionary patterns (1991) American Museum Novitates, 3025, pp. 1-23Devries, P.J., (1997) The Butterflies of Costa Rica and Their Natural History, 2, p. 327. , Riodinidae. Princeton University Press, PrincetonDevries, P.J., Baker, I., Butterfly exploitation of an ant-plant mutualism: Adding insult to herbivory (1989) Journal of The New York Entomological Society, 97, pp. 332-340Devries, P.J., Penz, C.M., Entomophagy, behavior, and elongated thoracic legs in the myrmecophilous Neotropical butterfly Alesa amesis (Riodinidae) (2000) Biotropica, 32, pp. 712-721Devries, P.J., Chacon, I.A., Murray, D., Toward a better understanding of host use biodiversity in riodinid butterflies (Lepidoptera) (1994) Journal of Research On the Lepidoptera, 31, pp. 103-126Devries, P.J., Cabral, B.C., Penz, C.M., The early stages of Apodemia paucipuncta (Riodinidae): Myrmecophily, a new ant-organ and consequences for classification (2004) Milwaukee Public Museum Contributions to Biology and Geology, 102, pp. 1-13Dutra, H.P., Freitas, A.V.L., Oliveira, P.S., Dual ant attraction in the neotropical shrub urera baccifera (Urticaceae): The role of ant visitation to pearl bodies and fruits in herbivore deterrence and leaf longevity (2006) Functional Ecology, 20, pp. 252-260Dyer, L.A., Tasty generalists and nasty specialists? antipredator mechanisms in tropical lepidopteran larvae (1995) Ecology, 76, pp. 1483-1496Dyer, L.A., Effectiveness of caterpillar defenses against three species of invertebrate predators (1997) Journal of Research On the Lepidoptera, 34, pp. 48-68Dyer, L.A., Bowers, M.D., The importance of sequestered iridoid glycosides as a defense against an ant predator (1996) Journal of Chemical Ecology, 22, pp. 1527-1539Dyer, L.A., Letourneau, D.K., Relative strengths of top-down and bottom-up forces in a tropical forest community (1999) Oecologia, 119, pp. 265-274Eastwood, R., Pierce, N.E., Kitching, R.L., Hughes, J.M., Do ants enhance diversification in lycaenid butterflies? Phylogeographic evidence from a model myrmecophile, Jalmenus evagoras (2006) Evolution, 60, pp. 315-327Ehrlich, P.R., Raven, P.H., Butterflies and plants: A study in coevolution (1964) Evolution, 18, pp. 586-608Eubanks, M.D., Nesci, K.A., Petersen, M.K., Liu, Z., Sanchez, A.B., The exploitation of an ant-defended host plant by a shelter-building herbivore (1997) Oecologia, 109, pp. 454-460Fiedler, K., Systematic, evolurionary, and ecological impli-cations of myrmecophily within the Lycaenidae (Insecta: Lepidop-tera: Papilionoidea) (1991) Bonner Zoologische Monographien, 31, pp. 1-201Fiedler, K., Lycaenid butterflies and plants: Is myrmecophily associated with amplified hostplant diversity? (1994) Ecological Entomology, 19, pp. 79-82Fiedler, K., Hölldobler, B., Ants and Polyommatus icarus immatures (Lycaenidae) - sex-related developmental benefits and costs of ant attendance (1992) Oecologia, 91, pp. 468-473Fiedler, K., Maschwitz, U., Functional analysis of the myrmecophilous relationships between ants (Hymenoptera: Formicidae) and lycaenids (Lepidoptera: Lycaenidae). II. Lycaenid larvae as trophobiotic partners of ants-a quantitative approach (1988) Oecologia, 75, pp. 204-206Fiedler, K., Saam, C., Ant benefit from attending facultatively myrmecophilous Lycaenidae caterpillars: Evidence from a survival study (1995) Oecologia, 104, pp. 316-322Floren, A., Biun, A., Linsenmair, K.E., Arboreal ants as key predators in tropical lowland rainforest trees (2002) Oecologia, 131, pp. 137-144Fraser, A.M., Axén, A.H., Pierce, N.E., Assessing the quality of different ant species as partners of a myrmecophilous butterfly (2001) Oecologia, 129, pp. 452-460Freitas, A.V.L., An anti-predator behavior in larvae of Libytheana carinenta (Nymphalidae, Libytheinae) (1999) Journal of The Lepidopterists' Society, 53, pp. 130-131Freitas, A.V.L., Oliveira, P.S., Biology and behavior of Eunica bechina (Lepidoptera: Nymphalidae) with special reference to larval defense against ant predation (1992) Journal of Research On the Lepidoptera, 31, pp. 1-11Freitas, A.V.L., Oliveira, P.S., Ants as selective agents on herbivore biology: Effects on the behaviour of a non-myrmecophilous butterfly (1996) Journal of Animal Ecology, 65, pp. 205-210Fukui, A., Indirect interactions mediated by leaf shelters in animal-plant communities (2001) Population Ecology, 43, pp. 31-40Gaston, K.J., Reavey, D., Valladares, G.R., Changes in feeding habit as caterpillars grow (1991) Ecological Entomology, 16, pp. 339-344Gentry, G.L., Dyer, L.A., On the conditional, nature of neotropical caterpillar defenses against their natural enemies (2002) Ecology, 83, pp. 3108-3119Gianoli, E., Sendoya, S., Vargas, F., Mejia, P., Jaffe, R., Rodriguez, M., Gutierrez, A., Patterns of Azteca ants' defence of Cecropia trees in a tropical rainforest: Support for optimal defence theory (2008) Ecological Research, 23, pp. 905-908Gross, P., Insect behavioral and morphological defenses against parasitoids (1993) Annual Review of Entomology, 38, pp. 251-273Harvey, D.J., (1987) The Higher Classification of The Riodinidae (lepidoptera), p. 215. , Ph.D. Dissertation, University of Texas, Austin, USAHeads, P.A., Lawton, J.H., Bracken, ants and extrafloral nectaries. 3. How insect herbivores avoid ant predation (1985) Ecological Entomology, 10, pp. 29-42Heil, M., Indirect defence via tritrophic interactions (2008) New Phytologist, 178, pp. 41-61Heil, M., McKey, D., Protective ant-plant interactions as model systems in ecological and evolutionary research (2003) Annual Review of Ecology Evolution and Systematics, 34, pp. 425-453Hojo, M.K., Wada-Katsumata, A., Akino, T., Yamaguchi, S., Ozaki, M., Yamaoka, R., Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae) (2008) Proceedings of The Royal Society of London B, , (doi: 10.1098/ rspb.2008.1064)Hölldobler, B., Communication between ants and their guests (1971) Scientific American, 224, pp. 86-93Hölldobler, B., Wilson, E.O., (1990) The Ants, p. 732. , Belknap Press/Harvard University Press, CambridgeHonda, K., Defensive potential of the larval osmeterial secretions of papilionid butterflies against ants (1983) Physiological Entomolology, 8, pp. 173-179Izzo, T.J., Vasconcelos, H.L., Cheating the cheater: Domatia loss minimizes the effects of ant castration in an Amazonian ant-plant (2002) Oecologia, 133, pp. 200-205Janzen, D.H., Coevolution of mutualism between ants and Acacias in Central America (1966) Evolution, 20, pp. 249-275Jolivet, P., Ants, plants, and beetlesa triangular relationship (1991) C.r. Huxley & D.f. Cutler, pp. 397-418. , (eds.). Ant-Plant Interactions. Oxford University Press, OxfordJones, M.T., Castellanos, I., Weiss, M.R., Do leaf shelters always protect caterpillars from invertebrate predators? (2002) Ecological Entomology, 27, pp. 753-757Kaminski, L.A., (2006) História Natural E Morfologia Dos Estágios Imaturos De Theope Thestias Hewitson, 1860 (lepidoptera, Riodinidae) Com Ênfase Na Mirmecofilia, p. 97. , M.Sc. Dissertation. Universidade Federal do Rio Grande do Sul, Porto Alegre, BrazilKaminski, L.A., Polyphagy and obligate myrmecophily in the butterfly Hallonympha paucipuncta (Lepidoptera: Riodinidae) in the Neotropical Cerrado savanna (2008) Biotropica, 40, pp. 390-394Kaminski, L.A., Immature stages of Caria plutargus (Lepidoptera: Riodinidae), with discussion on the behavioral and morphological defensive traits in nonmyrmecophilous riodinid butterflies (2008) Annals of The Entomological Society of America, 101, pp. 906-914Kaspari, M., Introduccion a la ecologia de las hormigas (2003) Introduccion a Las Hormigas De La Region Neotropical, pp. 97-112. , In: F. Fernandez (ed.), Instituto de Investigación de Recursos Biológicoa Alexandre von Humboldt, BogotáKoptur, S., Extrafloral nectary-mediated interactions between insects and plants (1992) Insect-plant Interactions, pp. 81-129. , In: E. Bernays (ed.), CRC Press, Boca RatonLenz, F., Kleinere mitteilungen. Der erhaltungsgrund der myrmekophilie (1917) Zeit. Induk. Abstamm. Vererbungsl, 18, pp. 44-48Lill, J.T., Marquis, R.J., Walker, M.A., Peterson, L., Ecological consequences of shelter sharing by leaf-tying caterpillars (2007) Entomologia Experimentalis Et Applicata, 124, pp. 45-53Loeffler, C.C., Caterpillar leaf folding as a defense against predation and dislodgment: Staged encounters using Dichomeius (Gelechiidae) larvae on goldenrods (1996) Journal of The Lepidopterists' Society, 50, pp. 245-260Machado, G., Freitas, A.V.L., Larval defence against ant predation in the butterfly Smyrna blomfildia (2001) Ecological Entomology, 26, pp. 436-439Machado, S.R., Morellato, L.P.C., Sajo, M.J., Oliveira, P.S., Morphological patterns of extrafloral nectaries in woody plant species of the Brazilian cerrado (2008) Plant Biology, 10, pp. 660-673Mackay, D.A., Whalen, M.A., Associations between ants (Hymenoptera: Formicidae) and Adriana Gaudich. (Euphorbiaceae) in East Gippsland (1998) Australian Journal of Entomology, 37, pp. 335-339Malicky, H., New aspects on the association between lycaenid larvae (Lycaenidae) and ants (Formicidae, Hymenoptera) (1970) Journal of The Lepidopterists' Society, 24, pp. 190-202Majer, J.D., The abundance and diversity of arboreal ants in Northern Australia (1990) Biotropica, 22, pp. 191-199Maschwitz, U., Schroth, M., Hänel, H., Tho, Y.P., Lycaenids parasitizing symbiotic plant-ant relationships (1984) Oecologia, 64, pp. 78-80Mega, N.O., Araújo, A.M., Do caterpillars of Dryas iulia alcionea (Lepidoptera, Nymphalidae) show evidence of adaptive behaviour to avoid predation by ants (2008) Journal of Natural History, 42, pp. 129-137Megens, H.J., de Jong, R., Fiedler, K., Phylogenetic patterns in larval host plant and ant association of Indo-Australian Arhopalini butterflies (Lycaenidae: Theclinae) (2005) Biological Journal of The Linnean Society, 84, pp. 225-241Mody, K., Linsenmair, K.E., Plant-attracted ants affect arthropod community structure but not necessarily herbivory (2004) Ecological Entomology, 29, pp. 217-225Morais, H.C., Coordinated group ambush: A new predatory behavior in Azteca ants (Dolichoderinae) (1994) Insectes Sociaux, 41, pp. 339-342Morellato, L.P.C., Oliveira, P.S., Distribution of extrafloral nectaries in different vegetation types of Amazonian Brazil (1991) Flora, 185, pp. 33-38Nash, D.R., Als, T.D., Maile, R., Jones, G.R., Boomsma, J.J., A mosaic of chemical coevolution in a large blue butterfly (2008) Science, 319, pp. 88-90Ness, J.H., Contrasting exotic Solenopsis invicta and native Forelius pruinosus ants as mutualists with Catalpa bignonioides, a native plant (2003) Ecological Entomology, 28, pp. 247-251Newcomer, E.J., Some observations on the relation of ants and lycaenid caterpillars, and a description of the relational organs of the latter (1912) Journal of The New York Entomological Society, 20, pp. 31-36Novotny, V., Basset, Y., Auga, J., Boen, W., Dal, C., Drozd, P., Kasbal, M., Molem, K., Predation risk for herbivorous insects on tropical vegetation: A search for enemy-free space and time (1999) Australian Journal of Ecology, 24, pp. 477-483Nylin, S., Janz, N., The ecology and evolution of host plant range: Butterflies as model group (1999) Herbivores: Between Plants and Predators, pp. 31-54. , In: H. Olff, U.K. Brown & M. Dres (eds.), Blackwell Science, LondonO'Dowd, D.J., Catchpole, E.A., Ants and extrafloral nectaries: No evidence for plant-protection in Helichrysum spp. ant interactions (1983) Oecologia, 59, pp. 191-200Ohsaki, N., Sato, Y., Food plant choice of Pieris butterflies as a trade-off between parasitoid avoidance and quality of plants (1994) Ecology, 75, pp. 59-68Oliveira, P.S., The ecological function of extrafloral nectaries: Herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae) (1997) Functional Ecology, 11, pp. 323-330Oliveira, P.S., Del-Claro, K., Multitrophic interactions in a Neotropical savanna: Ant-hemipteran systems, associated insect herbivores and a host plant (2005) Biotic Interactions In the Tropics, pp. 414-438. , In: D.F.R.P. Burslem, M.A. Pinard & S.E. Hartley (eds.), Cambridge university Press, CambridgeOliveira, P.S., Freitas, A.V.L., Ant-plant-herbivore interactions in the neotropical cerrado savanna (2004) Naturwissenschaften, 91, pp. 557-570Oliveira, P.S., Freitas, A.V.L., del-Claro, K., Ant foraging on plant foliage: Contrasting effects on the behavioral ecology of insects herbivores (2002) The Cerrados of Brazil: Ecology and Natural History of A Neotropical Savanna, pp. 287-305. , In: P.S. Oliveira & R.J. Marquis (eds.), Columbia University Press, New York, 398pOliveira, P.S., Leitão-Filho, H.F., Extrafloral nectaries: Their taxonomic distribution and abundance in the woody flora of Cerrado vegetation in Southeast Brazil (1987) Biotropica, 19, pp. 140-148Oliveira, P.S., Rico-Gray, V., Az-Castelazo, C., Castillo-Guevara, C., Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: Herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae) (1999) Functional Ecology, 13, pp. 623-631Oppenheim, S.J., Gould, F., Behavioral adaptations increase the value of enemy-free space for Heliothis subflexa, a specialist herbivore (2002) Evolution, 56, pp. 679-689Osborn, F.R., Jaffé, K., Chemical ecology of the defense of two Nymphalid butterfly larvae against ants (1998) Journal of Chemical Ecology, 24, pp. 1173-1181Penz, C.M., Devries, P.J., Systematic position of Apodemia paucipuncta (Riodinidae), and a critical evaluation of the nymphidiine transtilla (2006) Zootaxa, 1190, pp. 1-50Pierce, N.E., Amplified species diversity: A case study of an australian lycaenid butterfly and its attendant ants (1984) The Biology of Butterflies, pp. 197-200. , In: R.I. Wane-Wright & P.R. Ackery (eds.), Symposium of the Royal Entomological Society of London Number 11. Academic Press, LondonPierce, N.E., Predatory and parasitic Lepidoptera: Carnivores living on plants (1995) Journal of The Lepididopterists' Society, 49, pp. 412-453Pierce, N.E., Mead, M.A., Parasitoids as selective agents in the symbiosis between butterfly larvae and ants (1981) Science, 211, pp. 1185-1187Pierce, N.E., Elgar, M.A., The influence of ants on host plant selection by Jalmenus evagoras, a myrmecophilous lycaenid butterfly (1985) Behavior Ecolology and Sociobiology, 16, pp. 209-222Pierce, N.E., Kitching, R.L., Buckley, R.C., Taylor, M.F.J., Benbow, K.F., The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants (1987) Behavior Ecology and Sociobiology, 21, pp. 237-248Pierce, N.E., Nash, D.R., Baylis, M., Carper, E.R., Variation in the attractiveness of lycaenid butterfly larvae to ants (1991) Ant-plant Interactions, pp. 131-142. , In: C.R. Huxley & D.F. Cutler (eds.), Oxford University Press, OxfordPierce, N.E., Braby, M.F., Heath, A., Lohman, D.J., Mathew, J., Rand, D.B., Travassos, M.A., The ecology and evolution of ant association in the Lycaenidae (Lepidoptera) (2002) Annual Review of Entomology, 47, pp. 733-771Portugal, A.H.A., Trigo, J.R., Similarity of cuticular lipids between a caterpillar and its host plant: A way to make prey undetectable for predatory ants? (2005)

Mites Inhabiting A Lepidopteran Egg

[No abstract available]682141142Antor, R.J., García, M.B., A new mite-plant association: Mites living amidst the adhesive traps of a carnivorous plant (1995) Oecologia., 101 (1), pp. 51-54Braby, M.F., Nishida, K., The immature stages, larval food plants and biology of neotropical mistletoe butterflies. I. The Hesperocharis group (Pieridae: Anthocharidini) (2007) J. Lepid. Soc., 61 (4), pp. 181-195Dyar II, G., Notes on the larval-cases of Lacosomidae (Perophoridae) and life-history of Lacosoma chiridota Grt (1900) J. New York Entom. Soc., 8 (3), pp. 177-180Fournier, V., Rosenheim, J.A., Brodeur, J., Laney, L.O., Johnson, M.W., Herbivorous mites as ecological engineers: Indirect effects on arthropods inhabiting papaya foliage (2003) Oecologia., 135 (3), pp. 442-450Jones, C.G., Lawton II, J., Shachak, M., Organisms as ecosystem engineers (1994) Oikos, 69, pp. 231-386Kacata, H., Ohcushi, T., Leaf miner as a physical ecosy stem engineer: Secondary use of vacant leaf mines by other arthropods (2004) Ann. Entomol. Soc. Am., 97 (5), pp. 923-927Kaminski, L.A., Mota, L.L., Freitas, A.V.L., Moreira, G.R.P., Two ways to be a myrmecophilous butterfly: Natural history and comparative immature-stage morphology of two species of Theope (Lepidoptera: Riodinidae) (2013) Biol. J. Linn. Soc., 108, pp. 844-870Kawasaki, T., Yano, S., Osakabe, Mh., Effects of wall structure and light intensity on the settlement of a predatory mite, Eiiseius sojaensis (Ehara) (Acari: Phytoseudae) (2009) App. Entom. Zool., 44, pp. 81-84Lima, V.O., Demite, P.R., Vieira, C., Feres, R.J.F., Romero, G.Q., Contrasting engineering effects of leaf-rolling caterpillars on a tropical mite community (2013) Ecol. Entomol., 38, pp. 193-200O'Dowd, D.J., Willson, M.F., Leaf domatia and mites on Australasian plants: Ecological and evolutionary implications (1989) Biol. J. Linn. Soc., 37, pp. 191-236Peterson, A., Some types of eggs deposited by moths, Heterocera-Lepidoptera (1961) Fla. Entom., 44, pp. 107-114Peterson, A., Some eggs of moths among the Liparidae, Lasiocampidae, and Lacosomidae (Lepidoptera) (1966) Fla. Entom., 49, pp. 35-42Stehr, F.W., Order lepidoptera (1987) Immature insects., 1, pp. 288-596. , Stehr, F. W. ed., Kendall/Hunt Publishing Company, Dubuque, IowaVieira, C., Romero, G.Q., Ecosystem engineers on plants: Indirect facilitation of arthropod communities by leaf-rollers at different scales (2013) Ecology., 94, pp. 1510-1518Willson, M.R., Foliar shelters for mites in the Eastern Deciduous Forest (1991) Am. Midi. Nat., 126, pp. 111-11