Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiology ISSN: 0361-6525 DOI: 10.13102/sociobiology.v65i3.2843Sociobiology 65(3): 397-402 (September, 2018) Defensive Strategies of a Noctuid Caterpillar in a Myrmecophytic Plant: are Dyops Larvae Immune to Azteca Ants? Introduction As most holometabolous insects, Lepidoptera, one of the most diverse insect orders (Aguiar et al., 2009; Zhang, 2011), split their lives in distinct stages, enabling them to exploit different environments and diets. However, while adults are mobile and can easily escape from predators, lepidopteran larvae (caterpillars) present low mobility and usually feed on foliage, where vulnerability to natural enemies is high (Bernays, 1997). Together with birds, ants are the main predators of lepidopteran larvae (Remmel et al., 2011; Singer et al., 2012; Sendoya & Oliveira, 2017), and adults and larvae both exhibit a large array of strategies to avoid ant encounters (Salazar & Whitman, 2001; Freitas, 1999; Freitas & Oliveira, 1992, 1996; Machado & Freitas, 2001; Gentry & Dyer, 2002; Greeney et al., 2012; Sendoya & Oliveira, 2015, 2017). Anti-predator strategies may involve gregariousness (Turner & Pitcher, 1986; Lawrence, 1990; McClure & Despland Abstract Immature stages of insects are generally susceptive to their natural enemies, but many species developed defensive and evasive mechanisms to circumvent predation. Gregarious larvae of the noctuid moth Dyops cf. cuprescens feed on leaves of young Cecropia pachystachya shrubs colonized by Azteca ants. Ants avoid contact with larval clusters, retreating to the nest when larvae are moving near the stems. Provoked encounters revealed that Dyops caterpillars present several specialized behaviors to avoid and overcome ant attacks, such as fleeing to under leaf, jumping off the leaf, curling and wriggling vigorously the anterior portion of the body, spitting droplets of oral fluids, or killing ants by pouncing them. These mechanisms allow the caterpillars to overcome ant attacks and consume leaves of ant-colonized plants. By feeding on a heavily protected plant, larvae can enjoy not only a competitor-free plant, but possibly also the enemy-free space created by the aggressive ants. Sociobiology An international journal on social insects RR Ramos1, AVL Freitas1, RB Francini2 Article History Edited by Evandro N. Silva, UEFS, Brazil Received 10 January 2018 Initial acceptance 25 March 2018 Final acceptance 31 May 2018 Publication date 02 October 2018 Keywords Defensive behavior, larval behavior, insect-plant interaction, oral secretion, resource partitioning. Corresponding author Renato Rogner Ramos Departamento de Biologia Animal Instituto de Biologia Universidade Estadual de Campinas CEP 13083-862, Campinas-SP, Brasil. E-Mail: rognerramos@gmail.com 2011; Greeney et al., 2012), coloration such as camouflage and aposematism (Edmunds, 1974), morphological traits that make an enemy approach physically difficult, such as scoli, spines, and hairs (Frost, 1959), construction of protective shelters using plant tissue and faeces (Eubanks et al., 1997; Freitas, 1999; Freitas & Oliveira 1992, 1996; Machado & Freitas, 2001; Moraes et al., 2012), and the use of oral fluids to build circular barriers (DeVries, 1991). Gregarious larvae of the moth Dyops cf cuprescens Hampson (Noctuidae) use several species of Urticaceae as larval hostplant (Wiltshire, 1962, see also Janzen and Hallwachs, 2017, for pictures of early stages and host plant records), including Cecropia pachystachya Trécul (present study), a common myrmecophytic plant usually harboring colonies of Azteca ants (Formicidae: Dolichoderinae) in their hollow stems (Müller, 1881; Ihering, 1907). Azteca ants are known to prevent vines from climbing Cecropia trunks (Janzen, 1969; Schupp, 1986; Longino, 1991), and to attack 1 - Departamento de Biologia Animal and Museu de Zoologia, Universidade Estadual de Campinas, São Paulo, Brazil 2 - Universidade Católica de Santos, São Paulo, Brazil RESEARCH ARTICLE - ANTS RR Ramos, AV L Freitas, RB Francini – Defensive strategies of Dyops caterpillars against ants398 insect herbivores on leaves (Davidson 2005; Oliveira et al., 2015). Therefore, given that encounters between Dyops larvae and Azteca ants are expected to occur frequently on Cecropia foliage, we investigated the following questions: (1) Do Azteca ants attack Dyops larvae feeding on Cecropia leaves? (2) Do Dyops larvae present anti-predatory strategies to overcome ant attacks? Material and Methods The noctuid moth Dyops cf. cuprescens is a species widely distributed in the Neotropical region, occurring on the dry and humid Central American forests, in the Amazon and in the Atlantic Forest. Their caterpillars are gregarious and were reported using host plants mainly of the family Urticaceae (Wiltshire, 1962; Janzen & Hallwachs, 2017; Discover Life, 2018). Field observations and experiments were carried out in two areas of lowland dense ombrophilous forest (IBGE, 2012) on coastal São Paulo State, Southeastern Brazil: 1) Most of the study was undertaken at the “Vale do Rio Quilombo” (hereafter VQ), Santos municipality (further information in Francini 2010). Behavioral observations and simulated ant- caterpillar encounters in this site were carried out from April to May 2017. 2). Additional observations were carried out in the “Parque Estadual Xixová-Japui” (XJ), São Vicente municipality, from April to May 1992 (further information in Freitas, 1996). Encounters between Dyops and Azteca ants (n = 10) were provoked by gently removing one caterpillar (from 8 to 13 mm) from its cluster (n = 2 clusters) using a tweezer. The larva was then placed on the upper leaf surface of different individuals of C. pachystachya colonized by ants, categorized as follows: (1) the same plant where the larva was found (n = 4); (2) a different plant (same size and colonized by Azteca ants), not infested by Dyops larval clusters (n = 6). Experimental plants were gently shaken before each provoked encounter to incite ant activity on leaves. Ant-caterpillar interactions were recorded using two photographic cameras (Nikon Coolpix L5 and Canon 7D) and two video cameras (Go-Pro Hero 3 and Sony DSC HX300). Results Larvae of Dyops were always found in clusters containing 40 to 150 individuals (mean = 87.8, SD = 38.28, n = 7) on mature leaves of C. pachystachya (Fig 1A, B). All observed clusters were located on young plants (1 to 2 m tall) colonized by Azteca ants in both study sites, VQ (n = 2 clusters) and XJ (n = 5 clusters). In the beginning of our observations, despite the presence of larval clusters, all plants had most of their leaves intact. Ants appeared not to be disturbed by the presence of larval clusters, keeping distance as caterpillars fed and moved freely on foliage. Although larval clusters remained distant from the hollow Cecropia stems harboring the ant colonies most of the time, encounters with ants inevitably occurred whenever a cluster moved from one leaf to another. On these occasions, the larval cluster walked through the petiole and plant stem to reach a new leaf (Fig 1B). During these larval movements, ants retreated into the nest gallery and avoided contact with larvae. During the study period in VQ, Dyops-induced herbivory caused one Azteca-occupied Cecropia to have its leaves reduced from 10 to two in two weeks. A single observation of ant attack to a torn larva was observed, but the ant withdrew to the nest soon after the attack. Behavioral strategies of Dyops caterpillars to avoid ant attacks are summarized in Table 1. Nine out of 10 provoked encounters resulted in attacks by the ants (one larva was ignored on a plant hosting a cluster). Evasive behavior was by far the most observed, with larvae moving to under leaf ceasing its movements (n = 6). On two occasions the caterpillars jumped off the leaf upon attack, and suspended themselves on the end of a silken thread (Fig 1C). When attacked by ants (n = 7), Dyops caterpillars exhibited a “beat reflex” (n = 3), curling and wriggling vigorously the anterior portion of the body to dislodge or keep ants away, and/or spit oral fluids (n = 4) that effectively repelled the ants (Table 1). Oral fluids are expelled as drops of a transparent liquid that turns dark Behavior Description N Jumping off the leaf Larva drops off the plant after successive bites or attacks, falling on the soil or on a lower leaf of the same plant, or hanging themselves by silken threads (see below). 2 Dislodgment Larva moves to under leaf ceasing its movements; the larva usually is not followed by the ants. 6 Hanging from a silken thread The jumping larva can suspend itself by silken threads, eventually climbing back to leaf after a few minutes. 2 Spiting oral fluids Attacked larva raises the anterior portion of body and spits droplets of oral fluid towards the ants. 4 Safety zone Oral fluid falling on leaf surface forms moist patches that keep ants momentarily away (“safety perimeter”); ants touching these fluids showed several signs of disturbance such as body trembling, lethargy, rubbing the mandibles on leaf surface, and withdrawing stunned. 3 “Beat reflex” Curling and wriggling vigorously the anterior portion of the body can intimidate and temporarily keep ants away. 3 Pounce Pounce the ant simultaneously releasing oral fluid; ant dies almost instantly. 2 Table 1. Description of observed behavioral strategies of Dyops larvae to avoid attacks by Azteca ants on Cecropia pachystachya (from 10 provoked encounters). N = total number of observations of each behavior based on the 10 provoked encounters. Sociobiology 65(3): 397-402 (September, 2018) 399 after some minutes. These oral fluids falling on leaf surface form moist patches that keep ants away for several minutes, in a sort of “safety perimeter” (n = 3). Ants soaked by these oral fluids vigorously cleaned their mandibles, antennae and head, and some of which died after few minutes. Interestingly, ants that attached the caterpillar body ended up dying in few minutes (Fig 1D) after biting them. In addition, two larvae were observed displaying a pounce behavior, simultaneously biting and spitting fluids towards the ant, causing immediate death of the aggressor (see additional data on table 1) (a video clip showing most of the anti-predator behaviors is available at the following link: https://youtu.be/yHYiOQthFKg). See also a video as supplementary file: http://periodicos.uefs.br/index.php/sociobiology/rt/suppFiles/2843/0 http://dx.doi.org/10.13102/sociobiology.v65i3.2843.s1892 Discussion By living on a plant usually sheltering ant colonies, Dyops caterpillars display a series of anti-predator behaviors, as observed in other species feeding on plants where encounters with ants are frequent (Heads & Lawton, 1985; Bentley & Benson, 1988; Freitas & Oliveira, 1992, 1996; Oliveira & Freitas, 2004; Sendoya & Oliveira, 2015, 2017; Bächtold et al., 2012; Moraes et al., 2012). Most of the observed behaviors are common in non-myrmecophilous caterpillars, such as the “beat reflex”, biting, and jumping off the plant followed by hanging on a silken thread (Heads & Lawton, 1985; Salazar & Whitman, 2001; Sendoya & Oliveira, 2017). The behavior of spitting droplets of oral fluids against the aggressors is by far the most immediate anti- predation strategy observed in Dyops larvae. Regurgitation is a common anti-predation behavior in caterpillars in general (Freitas & Oliveira, 1992; Smedley et al., 1993; Gentry & Fig 1. A. Cluster of about 150 larvae of Dyops cf. cuprescens; B. A large larval cluster feeding on a nearly entire leaf (left arrow) after completely consuming a leaf (right arrow); note that a larval cluster must reach the main stem to reach a new leaf; C. A small larva (ca. of 1 cm) suspended by a silken thread after being attacked by ants; D. A medium sized larva (ca. of 3.5 cm) attacked by an ant that died later (white arrow); note the presence of brownish oral fluids beneath the larva. RR Ramos, AV L Freitas, RB Francini – Defensive strategies of Dyops caterpillars against ants400 Dyer, 2002), and its effectiveness to deter ant attacks has been already tested (Peterson et al., 1987; Rostas & Blassmann, 2009). In addition to the sub lethal effects observed when ants are soaked with oral fluids, Dyops larvae also displayed a very specialized pounce behavior that cause immediate death of the aggressors. The observation of dead ants attached to the body of attacked caterpillars suggests that larval fluids can be poisonous to ants (see also Collins, 2013), a defensive strategy that could be enhanced by gregariousness. However, further observations and experiments are needed to determine more precisely if the death of the ants attached to caterpillars’ bodies are caused by cuticle fluids, oral secretions, or bites by Dyops larvae upon attack. In short, although the present study do not include chemical analysis of the oral fluid of Dyops, the results strongly suggests that the oral fluids are not simple regurgitation of gut contents, as observed in other caterpillars and surely present noxious compounds that repel and protect the larvae against ants and other arthropod predators (Peterson et al., 1987; Rostas & Blassmann, 2009). In addition to the potential improvement of chemically- based ant deterrence, gregariousness is a defensive behavior by itself, where the group size and movement enhance the efficacy of defensive behaviors (Lawrence, 1990; McClure & Despland, 2011; Greeney et al., 2012). In fact, clusters of Dyops larvae were observed freely moving through various parts of C. pachystachya without being disturbed by ants, which retreat to their nest in the stem galleries when caterpillars approach, or are displaced to patrol plant sectors away from Dyops larval clusters. Additional observations in both study sites showed that, except for Dyops larvae, all other Cecropia herbivores are eliminated from plants after Azteca colonization. Interestingly, another species of Dyops (Dyops cf. cuprescens (Walker), was also observed in small Cecropia plants colonized by Azteca ants in the XJ site. However, larvae of this species are isolated and build shelters by curling the leaf edge under the leaf blade to form a tube (see Greeney & Jones, 2003). Further studies and experiments should be carried out to investigate if this species also present deterrence or other elaborate behaviors to escape from ant attacks. Our field observations indicate that gregarious larvae of Dyops can overcome the aggressiveness of Azteca ants inhabiting C. pachystachya, making it possible to feed on an ant-defended plant (Janzen, 1969; Schupp, 1986). In addition, by using a protected plant, larvae can enjoy not only a competitor-free plant, but possibly also an enemy-free space created by the aggressive ant inhabitants (see Price et al., 1980; Jeffries & Lawton, 1984; Kaminski et al., 2010; Dáttilo et al., 2016). Acknowledgements We would like to thank Dr. Victor O. Becker for helping with the identification of the Dyops caterpillars. Paulo S. Oliveira, Sebastian E. Sendoya and Lucas A. Kaminski kindly revised the last version of the manuscript. AVLF thanks the Brazilian CNPq (grant 303834/2015-3), RedeLep- SISBIOTA-Brasil/CNPq (563332/2010-7) and FAPESP (grant 2011/50225-3). References Aguiar, A.P., dos Santos, B.F., Couri, M.S., Rafael, J.A., Costa, C., Ide, S., Duarte, M., Grazia, J., Schwertner, C.F., Freitas, A.V.L. & Azevedo, C.O. (2009). Capítulo 8: Insecta. In R.M. Rocha & W.A.P. Boeger (Eds.), Estado da Arte e Perspectivas para a Zoologia no Brasil (pp. 131-155). Resultados dos Simpósios do XXVII Congresso Brasileiro de Zoologia. Curitiba: Editora UFPR. Bächtold, A., Del-Claro, K., Kaminski, L.A., Freitas, A.V.L. & Oliveira, P.S. (2012). Natural history of an ant-plant-butterfly interaction in a Neotropical savanna. Journal of Natural History, 46: 943-954. doi: 10.1080/00222933.2011.651649 Bentley, B.L. & Benson, W.W. (1988). The influence of ant foraging patterns on the behavior of herbivores. In J.C. Trager (ed.), Advances in Myrmecology (pp. 297-306), New York: E.J. Brill. Bernays, E.A. (1997). Feeding by lepidopteran larvae is dangerous. Ecological Entomology, 22: 121-123. doi: 10.1046/j.1365-2311.1997.00042.x Collins, M.M. (2013). On the finding of dead ants attached to Saturniid caterpillars: Evidence of successful deterrent chemistry? Journal of the Lepidopterists’ Society, 67: 62-63. doi: 10.18473/lepi.v67i1.a10 Dáttilo, W., Aguirre, A., Torre, P.L.L., Kaminski, L.A., Garcia- Chavez, J. & Rico-Gray, V. (2016). Trait-mediated indirect interactions of ant shape on the attack of caterpillars and fruits. Biology Letters, 12: 1-4. doi: 10.1098/rsbl.2016.0401 Davidson, D.W. (2005). Cecropia and its biotic defenses. In C.C. Berg & P.F. Rosselli (Eds.), Cecropia (pp. 214-226). Flora Neotropica Monograph. Bronx New York: The New York Botanical Garden. DeVries, P.J. (1991). Foam barriers, a new defense against ants for milkweed butterfly caterpillars (Nymphalidae: Danainae). The Journal of Research on the Lepidoptera, 30: 261-266. Discover Life (2018). Map center of Dyops cuprescens. http:// www.discoverlife.org/mp/20m?kind=Dyops+cuprescens (accessed date: 26 March 2018). Edmunds, M. (1974). Defence in Animals. A Survey of Anti- predator defences. Harlow, UK: Longman Group, 357 p Eubanks, M.D., Nesci, K.A., Petersen, M.K., Liu, Z. & Sanchez, A.B. (1997). The exploitation of an ant-defended host plant by a shelter-building herbivore. Oecologia, 109: 454-460. doi: 10.1007/s004420050105 Francini, R.B. (2010). História natural das borboletas do Vale Sociobiology 65(3): 397-402 (September, 2018) 401 do Rio Quilombo, Santos, SP, 2a. Edição. E-book arquivo PDF, Santos, SP, 550 p. doi: 10.13140/2.1.3862.9441 Freitas, A.V.L. (1996). Population biology of Heterosais edessa (Nymphalidae) and its associated Ithomiinae community. Journal of the Lepidopterists’ Society, 50: 273-289. Freitas, A.V.L. (1999). An anti-predator behavior in larvae of Libytheana carineta (Nymphalidae, Libytheinae). Journal of the lepidopterists’ Society, 53: 130-131. Freitas, A.V.L. & Oliveira, P.S. (1992). Biology and behavior of the neotropical butterfly Eunica bechina (Nymphalidae) with special reference to larval defence against ant predation. Journal of Research on the Lepidoptera, 31: 1-11. Freitas, A.V.L. & Oliveira, P.S. (1996). Ants as Selective Agents on Herbivore Biology: Effects on the Behaviour of a Non-Myrmecophilous Butterfly. Journal of Animal Ecology, 65: 205-210. Frost, S.W. (1959). Insect Life and Natural History. New York, Dover, 526 p Gentry, G.L. & Dyer, L.A. (2002). On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology, 83: 3108-3119. doi: 10.1890/0012-9658(2002)083[3108:OTCNON]2.0.CO;2 Greeney, H. F. & Jones, M.T. (2003). Shelter building in the Hesperiidae: a classification scheme for larval shelters. Journal of Research on the Lepidoptera, 37: 27-36. Greeney, H.F., Dyer, L.A. & Smilanich, A.M. (2012). Feeding by lepidopteran larvae is dangerous: A review of caterpillars’ chemical, physiological, morphological, and behavioral defenses against natural enemies. Invertebrate Survival Journal, 9: 7-34. Retrieved from: http://www.isj. unimo.it/articoli/ISJ256.pdf Heads, P.A. & Lawton J.H. (1985). Braken, ants and extrafloral nectaries. III. How insect hebivores avoid ant predation. Ecological Entomology, 10: 29-42. doi: 10.1111/j.1365- 2311.1985.tb00532.x IBGE, (2012). Manual Técnico da Vegetação Brasileira. Instituto Brasileiro de Geográfica e Estatística Rio de Janeiro: IBGE, 275 p Ihering, H. (1907). Die Cecropien und ihre Schutzameisen. Engler’s Botanische Jahrbücher, 39: 666-714. Janzen, D. H. 1969. Allelopathy by myrmecophytes: The ant Azteca as an allelopathic agent of Cecropia. Ecology, 50: 147-153. Janzen, D.H. & Hallwachs, W. (2017). Dynamic Database for an Inventory of the Macrocaterpillar Fauna, and its Food Plants and Parasitoids, of the Area De Conservacion Guanacaste, Northwestern Costa Rica. University of Pennsylvania, Philadelphia, PA. http://janzen.sas.upenn.edu/caterpillars/ database.lasso (accessed date: 28 December 2017). Jeffries, M.J. & Lawton, J.H. (1984). Enemy free space and the structure of ecological communities. Biological Journal of the Linnean Society, 23: 269-286. doi: 10.1111/j.1095- 8312.1984.tb00145.x Kaminski, L.A., Freitas A.V.L. & Oliveira P.S. (2010). Interaction between mutualisms: Ant-tended butterflies exploit enemy-free space provided by ant-treehopper associations. American Naturalist, 176: 322-334. doi: 10.1086/655427 Lawrence, W.S. (1990). The effects of group-size and host species on development and survivorship of a gregarious caterpillar Halisidota caryae (Lepidoptera, Arctiidae). Ecological Entomology, 15: 53-62. doi: 10.1111/j.1365-2311.1990.tb00783.x Longino, J.T. (1991). Azteca ants in Cecropia trees: taxonomy, colony structure, and behavior. In D. Cutler & C. Huxley (Eds.), Ant-Plant Interactions (pp. 271-288). Oxford: Oxford University Press. Machado, G. & Freitas, A.V.L. (2001). Larval defence against ant predation in the butterfly Smyrna blomfildia. Ecological Entomology, 26: 436-439. doi: 10.1046/j.1365- 2311.2001.00328.x McClure, M. & Despland, E. (2011). Defensive responses by a social caterpillar are tailored to different predators and change with larval instar and group size. Naturwissenschaften, 98(5): 425-434. doi: 10.1007/s00114-011-0788-x Moraes, A.R., Greeney, H.F., Oliveira, P.S., Barbosa, E.P. & Freitas, A.V.L. (2012). Morphology and behavior of the early stages of the skipper, Urbanus esmeraldus, on Urera baccifera, an ant-visited host plant. Journal of Insect Science, 12: 52. doi: 10.1673/031.012.5201 Müller, F. (1881). Die Imbauba und ihre Beschuetzer. Kosmos, 8:109-116. Oliveira, K.N., Coley, P.D., Kursar, T.A., Kaminski, L.A., Moreira, M.Z. & Campos, R.I. (2015). The effect of symbiotic ant colonies on plant growth: a test using an Azteca-Cecropia System. PLOS ONE 10 (3): e0120351. doi: 10.1371/journal. pone.0120351 Oliveira, P.S. & Freitas, A.V.L. (2004). Ant-plant- herbivore interactions in the Neotropical Cerrado savanna. Naturwissenschaften, 91: 557-570. doi: 10.1007/s00114-004- 0585-x Peterson, S.C., Johnson, N.D. & LeGuyader, J.L. (1987). Defensive regurgitation of allelochemicals derived from host cyanogenesis by eastern tent caterpillars. Ecology, 68: 1268- 1272. doi: 10.2307/1939211 Price, P.W., Bouton, C.E., Gross, P., Mcpheron, B.A., Thompson, J.N. & Weis, A.E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics, 11: 41-65. doi: 10.1146/annurev.es.11.110180.000353 RR Ramos, AV L Freitas, RB Francini – Defensive strategies of Dyops caterpillars against ants402 Remmel, T., Davison, J. & Tammaru, T. (2011). Quantifying predation on folivorous insect larvae: the perspective of life- history evolution. Biological Journal of the Linnean Society, 104: 1-18. doi: 10.1111/j.1095-8312.2011.01721.x Rostas, M. & Blassmann, K. (2009). Insects had it first: Surfactants as a defense against predators. Proceedings of the Royal Society B, 276: 633-638. doi: 10.1098/rspb.2008.1281 Salazar, B.A. & Whitman, D.W. (2001). Defensive tactics of caterpillars against predators and parasitoids. In T.N. Ananthakrishnan (Ed.), Insects and Plant Defences Dynamics (pp. 161-207). Plymouth, UK: Science Publishers, Inc. Sendoya, S.F. & Oliveira, P.S. (2015). Ant-caterpillar antagonism at the community level: interhabitat variation of tritrophic interactions in a neotropical savanna. Journal of Animal Ecology, 84: 442-452. doi: 10.1111/1365-2656.12286 Sendoya, S.F. & Oliveira, P.S. (2017). Behavioural ecology of defence in a risky environment: caterpillars versus ants in a Neotropical savanna. Ecological Entomology, 42: 553-564. doi: 10.1111/een.12416 Schupp, E.W. (1986). Azteca protection of Cecropia: Ant occupation benefits juvenile trees. Oecologia, 70: 379-385. doi: 10.1007/BF00379500 Smedley, S.R., Ehrhardt, E. & Eisner, T. (1993). Defensive regurgitation by a noctuid moth larva (Litoprosopus futilis). Psyche: A Journal of Entomology, 100: 209-221. doi: 10.1155/1993/67950 Singer, M.S., Farkas, T.E., Skorik, C.M. & Mooney, K.A. (2012). Tritrophic interactions at a community level: effects of host plant species quality on bird predation of caterpillars. American Naturalist, 179: 363-374. doi: 10.1086/664080 Turner, G.F. & Pitcher, T.J. (1986). Attack abatement: a model for group protection by combined avoidance and dilution. The American Naturalist, 128: 228-240. doi: 10.1086/284556 Wiltshire, E.P. (1962). Notes on Neotropical Lepidoptera. 1. The early stages and comparative morphology of two species of Dyops (Noctuidae) hitherto confused. Journal of the Lepidopterists’ Society, 16: 47-54. Zhang, Z.-Q. (2011). Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148: 1-237.