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Contrast to background influences predation on aposematic but not cryptic artificial caterpillars in a Brazilian coastal shrubland

Published online by Cambridge University Press:  30 April 2020

Rayane S. Oliveira
Affiliation:
Programa de Pós-graduação em Ecologia de Ecossistemas, Universidade Vila Velha, ES, Brazil Laboratório de Ecologia de Populações e Conservação, Universidade Vila Velha, ES, Brazil
Pedro Diniz
Affiliation:
Programa de Pós-graduação em Ecologia de Ecossistemas, Universidade Vila Velha, ES, Brazil Programa de Pós-Graduação em Ecologia, Universidade de Brasília, DF, Brazil
Vitor Araujo-Lima
Affiliation:
Programa de Pós-graduação em Ecologia de Ecossistemas, Universidade Vila Velha, ES, Brazil
Gabriela Rosário
Affiliation:
Laboratório de Ecologia de Populações e Conservação, Universidade Vila Velha, ES, Brazil
Charles Duca*
Affiliation:
Laboratório de Ecologia de Populações e Conservação, Universidade Vila Velha, ES, Brazil
*
Author for correspondence: *Charles Duca, Email: cduca@uvv.br

Abstract

Aposematism and crypticity are visual defensive strategies against predation; however, the relative effectiveness of these two strategies to reduce the risk of predation is not yet fully understood. We evaluated the risk of predation for caterpillars with cryptic and aposematic colouration as well as the probability of predation relative to the natural variation of contrast with the substrate. We expected that the two models would experience similar predation attempts and that the contrast with the substrate would be negatively related to the predation on aposematic mimic models and positively to the predation of cryptic models. Overall, 224 models were laid out along a transect and exposed to predation for five consecutive days during winter and autumn. Daily predation was 11.0% (winter) and 4.8% (autumn). Significant differences were not observed between predation rates on the two model types (50.6% aposematic). Most of the predated models had arthropod marks (86.4%) and only 13.6% had bird marks. The chance of predation was higher the greater the contrast between the aposematic mimic model and the substrate, although no relationship was observed for the cryptic model. Our results suggest that the two colour patterns do not differ in their defensive effectiveness and that micro-habitat selection might define the predation risk on aposematic mimic caterpillars in environments dominated by arthropod predators.

Type
Research Article
Copyright
© The Author(s) 2020. Published by Cambridge University Press

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References

Literature cited

Alvares, CA, Stape, JL, Sentelhas, PC, De Moraes Gonçalves, JL and Sparovek, G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22, 711728.CrossRefGoogle Scholar
Akkaynak, D, Allen, JJ, Mäthger, LM, Chiao, CC and Hanlon, RT (2013) Quantification of cuttlefish (Sepia officinalis) camouflage: a study of color and luminance using in situ spectrometry. Journal of Comparative Physiology A 199, 211225.CrossRefGoogle ScholarPubMed
Arenas, LM, Troscianko, J and Stevens, M (2014) Color contrast and stability as key elements for effective warning signals. Frontiers in Ecology and Evolution 2,112.CrossRefGoogle Scholar
Arnold, SE, Stevenson, PC and Belmain, ST (2016) Shades of yellow: interactive effects of visual and odour cues in a pest beetle. Journal of Life and Environmental Sciences. doi: 10.7717/peerj.2219.Google Scholar
Aronsson, M and Gamberale-Stille, G (2009) Importance of internal pattern contrast and contrast against the background in aposematic signals. Behavioral Ecology 20, 13561362.CrossRefGoogle Scholar
Ayres, SM and Ayres-Jr, M (2007) BioEstat: Aplicações estatísticas nas áreas de ciências biomédicas. Belém: Instituto de Desenvolvimento Sustentável Mamirauá 5, 1339.Google Scholar
Barnett, JB, Constantine, M, Scott-Samnuel, NE and Cuthiill, IC (2018) Distance-dependent defensive coloration in the poison frog Dendrobates tinctorius, Dendrobatidae. Proceedings of the National Academy of Sciences USA 115, 64166421.CrossRefGoogle ScholarPubMed
Bergeron, ZT and Fuller, RC (2018) Using human vision to detect variation in avian coloration: how bad is it? American Naturalist 191, 269276.CrossRefGoogle Scholar
Bianchini, E and Santos, FA (2005) Herbivoria foliar em Chrysophyllum gonocarpum (Sapotaceae) no Parque Estadual Mata dos Godoy, Londrina, estado do Paraná, Brasil. Acta Scientiarum – Biological Sciences 27, 285290.CrossRefGoogle Scholar
Caro, T and Ruxton, G (2019) Aposematism: unpacking the defences. Trends in Ecology & Evolution. doi: 10.1016/j.tree.2019.02.015.CrossRefGoogle ScholarPubMed
Caro, T, Sherratt, TN and Stevens, M (2016) The ecology of multiple colour defences. Evolutionary Ecology 30, 797809.CrossRefGoogle Scholar
Carroll, J and Sherratt, TN (2013) A direct comparison of the effectiveness of two anti-predator strategies under field conditions. Journal of Zoology 291, 279285.CrossRefGoogle Scholar
Dell’Aglio, DD, Stevens, M and Jiggins, CD (2016) Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest. Ecological Entomology 41, 627632.CrossRefGoogle Scholar
Dyer, LA (1997) Effectiveness of caterpillar defenses against three species of invertebrate predators. Journal of Research on the Lepidoptera 34, 4868.Google Scholar
Endler, JA (1978) A predator’s view of animal color patterns. In Hecht, MK, Steere, WC and Wallace, B (eds) Evolutionary Biology. Boston: Springer, pp. 19761977.Google Scholar
Endler, JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biological Journal of the Linnean Society 41, 315352.CrossRefGoogle Scholar
Exnerová, A, Stys, P, Fucilokova, E, Veselá, S, Svádová, K, Prokopová, M, Jarosik, V, Fuchs, R and Landová, E (2006) Avoidance of aposematic prey in European tits (Paridae): learned or innate? Ecology 18, 148156.Google Scholar
Ferrante, M, Barone, G, Kiss, M, Bozóné-Borbáth, E and Lövei, GL (2017) Ground-level predation on artificial caterpillars indicates no enemy-free time for lepidopteran larvae. Community Ecology 18, 280286.CrossRefGoogle Scholar
Gaitonde, N, Joshi, J and Kunte, K (2018) Evolution of ontogenic change in color defenses of swallowtail butterflies. Ecology and Evolution 8, 97519763.CrossRefGoogle ScholarPubMed
Gendron, RP and Staddon, JER (1983) Searching for cryptic prey: the effect of search rate. American Society of Naturalists 121, 172186.CrossRefGoogle Scholar
Greeney, HF, Dyer, LA and Smilanich, AM (2012). Feeding by lepidopteran larvae is dangerous: a review of caterpillars’ chemical, physiological, morphological, and behavioral defenses against natural enemies. Invertebrate Survival Journal 9, 734.Google Scholar
Heinrich, B and Collins, SL (1983) Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64, 592602.CrossRefGoogle Scholar
Howe, A, Lövei, GL and Nachman, G (2009) Dummy caterpillars as a simple method to assess predation rates on invertebrates in a tropical agroecosystem. Entomologia Experimentalis et Applicata 131, 325329.CrossRefGoogle Scholar
Iniesta, LFM, Ratton, P and Guerra, TJ (2017) Avian predators avoid attacking artificial aposematic millipedes in Brazilian Atlantic Forest. Journal of Tropical Ecology 33, 8993.CrossRefGoogle Scholar
Langellotto, GA and Denno, RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139, 110.CrossRefGoogle ScholarPubMed
Lindstedt, C, Boncoraglio, G, Cotter, S, Gilbert, J and Kilner, RM (2017) Aposematism in the burying beetle? Dual function of anal fluid in parental care and chemical defense. Behavioral Ecology 28, 14141422.CrossRefGoogle Scholar
Long, CV, Flint, JA and Lepper, PA (2011) Insect attraction to wind turbines: does colour play a role? European Journal of Wildlife Research 57, 323331.CrossRefGoogle Scholar
Lövei, GL and Ferrante, M (2017) A review of the sentinel prey method as a way of quantifying invertebrate predation under field conditions. Insect Science 24, 528542.CrossRefGoogle ScholarPubMed
Low, PA, Sam, K, McArthur, C, Posa, MRC and Hochuli, DF (2014) Determining predator identity from attack marks left in model caterpillars: guidelines for best practice. Entomologia Experimentalis et Applicata 152, 120126.CrossRefGoogle Scholar
Lucchetta, P, Bernstein, C, Théry, M, Lazzari, C and Desouhant, E (2008) Foraging and associative learning of visual signals in a parasitic wasp. Animal Cognition 11, 525533.CrossRefGoogle Scholar
Magnago, LFS, Martins, SV and Pereira, OJ (2011) Heterogeneidade florística das fitocenoses de restingas nos estados do Rio de Janeiro e Espírito Santo, Brasil. Revista Árvore 35, 245254.CrossRefGoogle Scholar
Marples, NM and Mappes, J (2011) Can the dietary conservatism of predators compensate for positive frequency dependent selection against rare, conspicuous prey? Evolutionary Ecology 25, 737749.CrossRefGoogle Scholar
Poch, TJ and Simonetti, JA (2013) Insectivory in Pinus radiata plantations with different degree of structural complexity. Forest Ecology and Management 304, 132136.CrossRefGoogle Scholar
Porter, SS (2013) Adaptive divergence in seed color camouflage in contrasting soil environments. New Phytologist 197, 13111320.CrossRefGoogle ScholarPubMed
Quintero, C and Bowers, MD (2018) Plant and herbivore ontogeny interact to shape the preference, performance and chemical defense of a specialist herbivore. Oecologia 187, 401412.CrossRefGoogle ScholarPubMed
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Roslin, T, Hardwick, B, Novotny, V, Petry, WK, Andrew, NR, Asmus, A, Barrio, IC, Basset, Y, Boesing, AL, Bonebrake, CT, Cameron, EK, Dáttilo, W, Donoso, DA, Drozd, P, Gray, CL, Kik, DS, Hill, SJ, Hopkins, T, Huand, S, Koane, B, Laird-Hopkins, B, Laukkanen, L, Lewis, OT, Milne, S, Isaiah, M, Nakamura, A, Nell, CS, Nichols, E, Prokurat, A, Katerina, S, Schmidt, NM, Slade, A, Slade, V, Suchanková, A, Teder, T, Nouhuys, S, Vandvik, V, Weissflog, A, Zhukovich, V and Slade, EM (2017) Higher predation risk for insect prey at low latitudes and elevations. Science 356, 742744.CrossRefGoogle ScholarPubMed
Ruxton, GD, Sherratt, TN and Speed, MP (2004) The evolution and maintenance of Müllerian mimicry. In Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. Oxford: Oxford University Press, pp. 248450.CrossRefGoogle Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671675.CrossRefGoogle ScholarPubMed
Seifert, CL, Schulze, CH, Dreschke, TCT, Frötscher, H and Fiedler, K (2016) Day vs. night predation on artificial caterpillars in primary rainforesthabitats – an experimental approach. Entomologia Experimentalis et Applicata 158, 5459.CrossRefGoogle Scholar
Stevens, M and Ruxton, GD (2012) Linking the evolution and form of warning coloration in nature. Proceedings of the Royal Society B: Biological Sciences 279,417426.CrossRefGoogle ScholarPubMed
Stevens, M, Párraga, CA, Cuthill, IC, Partridge, JC and Troscianko, TS (2007) Using digital photography to study animal coloration. Biological Journal of the Linnean Society 90, 211237.CrossRefGoogle Scholar
Tvardikova, K and Novotny, V (2012) Predation on exposed and leaf-rolling artificial caterpillars in tropical forests of Papua New Guinea. Journal of Tropical Ecology 28, 331341.CrossRefGoogle Scholar