Despland, Emma (2019) Caterpillars Cooperate to Overcome Plant Glandular Trichome Defenses. Frontiers in Ecology and Evolution, 7 . ISSN 2296-701X
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Official URL: http://dx.doi.org/10.3389/fevo.2019.00232
Abstract
One common advantage proposed for group-living in animals is social facilitation of feeding, by which food acquisition by an individual is made easier by feeding neighbors. The present paper provides an explanation of social facilitation of feeding in a gregarious leaf-chewing insect, demonstrating how caterpillars cooperate to overwhelm plant trichome defenses and pierce a hole in the leaf on which they feed collectively. Specifically, it tests the hypotheses that Mechanitis menapis caterpillars feed collectively, that the glandular trichomes of Solanum acerifolium are effective defenses against this specialist herbivore, and that feeding by early-instar M. menapis is socially facilitated in the presence of glandular trichomes. A field survey showed that Mechanitis menapis on trichome–bearing plants feed collectively on the abaxial surface of leaves during the first larval instars. In a lab experiment comparing feeding on control and ethanol-washed leaves, caterpillars on the glandular-trichome-free washed sides of leaves initiated feeding sooner and had higher survival rates, suggesting that glandular trichomes are effective defenses. Behavioral observations showed that feeding is socially facilitated in response to glandular trichomes: caterpillars on the washed sides of leaves were more likely to begin feeding alone and initiated more separate feeding sites, suggesting that caterpillars are less able to initiate feeding independently in the presence of glandular trichomes. These results demonstrate a novel mechanism of cooperation among folivores, showing how they can benefit from grouping to tackle food sources that would be unavailable to isolated individuals. This study thus demonstrates that social facilitation of feeding extends to insect folivores, a hyper-diverse and abundant feeding guild.
Divisions: | Concordia University > Faculty of Arts and Science > Biology |
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Item Type: | Article |
Refereed: | Yes |
Authors: | Despland, Emma |
Journal or Publication: | Frontiers in Ecology and Evolution |
Date: | 2019 |
Funders: |
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Digital Object Identifier (DOI): | 10.3389/fevo.2019.00232 |
Keywords: | plant-insect interactions, group-living, lepidoptera, aggregation, social facilitation, cooperation, solanaceae, collective foraging |
ID Code: | 986085 |
Deposited By: | Krista Alexander |
Deposited On: | 13 Nov 2019 21:51 |
Last Modified: | 13 Nov 2019 21:51 |
References:
Allen, P. E. (2010). Group size effects on survivorship and adult development in the gregarious larvae of Euselasia chrysippe (Lepidoptera, Riodinidae). Insec. Soc. 57, 199–204. doi: 10.1007/s00040-010-0068-3Arantes, A. H. (2001). Defensa química em larvas da borboleta Mechanitis polymnia (Nymphalidae: Ithomiinae). Ph.D. thesis, Instituto de Biologia, Universidade Estadual de Campinas, Brazil.
Barker, J. L., Bronstein, J. L., Friesen, M. L., Jones, E. I., Reeve, H. K., Zink, A. G., et al. (2017). Synthesizing perspectives on the evolution of cooperation within and between species. Evolution 71, 814–825. doi: 10.1111/evo.13174
Boligon, D., and Medeiros, L. (2007). Adaptations of two specialist herbivores to movement on the hairy leaf surface of their host, Solanum guaraniticum hassl (Solanaceae). Rev. Brasil. Entomol. 51, 210–216. doi: 10.1590/S0085-56262007000200011
Brown, K. S., and Freitas, A. V. L. (1994). Juvenile stages of Ithomiinae: Overview and systematics (Lepidoptera: Nymphalidae). Trop. Lepidopter. 5, 9–20.
Clark, B. R., and Faeth, S. H. (1997). The consequences of larval aggregation in the butterfly Chlosyne lacinia. Ecol. Entomol. 22, 408–415. doi: 10.1046/j.1365-2311.1997.00091.x
Clissold, F. (2008). “The biomechanics of chewing and plant fracture: mechanisms and implications,” in Advances in Insect Physiology: Insect Mechanics and Control, eds J. Casas and S. J. Simpson (London, Academic Press), 317–372.
Cornell, J. C., Stamp, N. E., and Bowers, D. (1987). Developmental change in aggregation, defense and escape behavior of buckmoth caterpillars, Hemileuca lucina (Saturniidae). Behav. Ecol. Sociobiol. 20, 383–388. doi: 10.1007/BF00302980
Costa, J. T. (2006). The Other Insect Societies. Cambridge: Belknap Press.
Costa, J. T., and Pierce, N. E. (1997). “Social evolution in the Lepidoptera: ecological context and communication in larval societies,” in The Evolution of Social Behaviour in Insects and Arachnids, eds J. C. Choe and B. J. Crespi (Cambridge: Cambridge University Press), 407–442. doi: 10.1017/CBO9780511721953.021
Denno, R. F., and Benrey, B. (1997). Aggregation facilitates larval growth in the neotropical nymphalid butterfly Chlosyne janais. Ecol. Entomol. 22, 133–141. doi: 10.1046/j.1365-2311.1997.t01-1-00063.x
Despland, E. (2018). Effects of phenological synchronization on caterpillar early-instar survival under a changing climate. Can. J. Forest Res. 48, 247–254. doi: 10.1139/cjfr-2016-0537
Despland, E., and Santacruz-Endara, P. (2016). Silk drives aggregation and following in the neotropical Ithomiine caterpillar Mechanitis menapis. Physiol. Entomol. 41, 274–280. doi: 10.1111/phen.12153
Fiorentino, V. L., Murphy, S. M., Stoepler, T. M., and Lill, J. T. (2014). Facilitative effects of group feeding on performance of the saddleback caterpillar (Lepidoptera: Limacodidae). Environ. Entomol. 43, 131–138. doi: 10.1603/EN13144
Fitzgerald, T. D., and Costa, J. T. (1999). “Collective behavior in social caterpillars,” in Information Processing in Social Insects, eds C. Detrain, J. L. Deneubourg, and J. M. Pasteels (Basel: Birkhaüser Verlag, 379–400.
Fordyce, J. A., and Agrawal, A. A. (2001). The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor. J. Anim. Ecol. 70, 997–1005. doi: 10.1046/j.0021-8790.2001.00568.x
Giraldeau, L. A., and Caraco, T. (2000). Social Foraging Theory. Princeton: Princeton University Press. doi: 10.1515/9780691188348
Giraldo, C. E., and Uribe, S. I. (2010). Registro de Mechanitis polymnia (Lepidoptera: Ithomiinae) en Solanum jamaicense y ciclo de vida en laboratorio. Revis. Colomb. Entomol. 36, 165–168. Available online at: http://www.scielo.org.co/scielo.php?pid=S0120-04882010000100025&script=sci_arttext&tlng=en
Giraldo, C. E., and Uribe, S. I. (2012). Taxonomy of Mechanitis (F.) (Lepidoptera: Nymphalidae) from the west Colombian Andes: an integrative approach. Neotr. Entomol. 41, 472–484. doi: 10.1007/s13744-012-0071-7
Gurr, G. M., and McGrath, D. (2001). Effect of plant variety, plant age and photoperiod on glandular pubescence and host-plant resistance to potato moth (Phthorimaea operculella) in Lycopersicon spp. Ann. Appl. Biol. 138, 221–230. doi: 10.1111/j.1744-7348.2001.tb00106.x
Gurr, G. M., and McGrath, D. (2002). Foliar pubescence and resistance to potato moth, Phthorimaea operculella, in Lycopersicon hirsutum. Entomol. Exp. Appl. 103, 35–41. doi: 10.1046/j.1570-7458.2002.00960.x
Hulley, P. E. (1988). Caterpillar attacks plant mechanical defence by mowing trichomes before feeding. Ecol. Entomol. 13, 239–241. doi: 10.1111/j.1365-2311.1988.tb00351.x
Inouye, B. D., and Johnson, D. M. (2005). Larval aggregation affects feeding rate in Chlosyne poecile (Lepidoptera: Nymphalidae). Florida Entomol. 88, 247–252. doi: 10.1653/0015-4040(2005)088[0247:LAAFRI]2.0.CO;2
Johnson, S. N., Clark, K. E., Hartley, S. E., Jones, T. H., McKenzie, S. W., and Koricheva, J. (2012). Aboveground–belowground herbivore interactions: a meta-analysis. Ecology 93, 2208–2215. doi: 10.1890/11-2272.1
Kariyat, R. R., Hardison, S. B., Ryan, A. B., Stephenson, A. G., De Moraes, C. M., and Mescher, M. C. (2018). Leaf trichomes affect caterpillar feeding in an instar-specific manner. Commun. Integr. Biol. 11, 1–6. doi: 10.1080/19420889.2018.1486653
Lawrence, W. S. (1990). The effects of group size and host species on development and survivorship of a gregarious caterpillar, Halisidota carye (lepidoptera: Arctiidae). Ecol. Entomol. 15, 53–62. doi: 10.1111/j.1365-2311.1990.tb00783.x
Levin, D. A. (1973). The role of trichomes in plant defense. Q. Rev. Biol. 48, 3–15. doi: 10.1086/407484
Levin, R. A., Myers, N. R., and Bohs, L. (2006). Phylogenetic relationships among the “spiny solanums” (Solanum subgenus Leptostemonum, Solanaceae). Am. J. Botany 93, 157–169. doi: 10.3732/ajb.93.1.157
McMillen, J. D., and Wagner, M. R. (1998). Influence of host plant vs. natural enemies on the spatial distribution of a pine sawfly, Neodiprion autumnalis. Ecol. Entomol. 23, 397–383. doi: 10.1046/j.1365-2311.1998.00146.x
Nahrung, H. F., Dunstan, P. K., and Allen, G. R. (2001). Larval gregariousness and neonate establishment of the eucalypt-feeding beetle Chrysophtharta agricola (Coleoptera: Chrysomelidae: Paropsini). Oikos 98, 358–364. doi: 10.1034/j.1600-0706.2001.940217.x
Pescador-Rubio, A. (2009). Growth and survival of a tropical polyphagous caterpillar: effects of host and group size. Southwestern Entomol. 34, 75–84. doi: 10.3958/059.034.0107
Prokopy, R. J., and Roitberg, B. D. (2001). Joining and avoidance behavior in nonsocial insects. Annu. Rev. Entomol. 46, 631–365. doi: 10.1146/annurev.ento.46.1.631
Raffa, K., Aukema, B., Bentz, B., Carroll, A., Hicke, J., Turner, M., et al. (2008). Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. Bioscience 58, 501–517. doi: 10.1641/B580607
Rathcke, B. J., and Poole, R. W. (1975). Coevolutionary race continues: butterfly larval adaptation to plant trichomes. Science 187, 175–176. doi: 10.1126/science.187.4172.175
Reader, T., and Hochuli, D. (2003). Understanding gregariousness in a larval Lepidopteran: the roles of host plant, predation, and microclimate. Ecol. Entomol. 28, 729–737. doi: 10.1111/j.1365-2311.2003.00560.x
Robinson, G. S., Ackery, P. R., Kitching, I. J., Beccaloni, G. W., and Hernández, L. M. (2010). HOSTS - A Database of the World's Lepidopteran Hostplants. London: Natural History Museum. Available online at: http://Www.nhm.ac.uk/hosts.~2018
Santacruz-Endara, P. (2012). Historia Natural, Ciclo de Vida y Parasitismo de la Mariposa Mechanitis Menapis Mantineus. Licencia Biologia, Pontificia Universidad Católica del Ecuador.
Schoonhoven, L. M., van Loon, J. J. A., and Dicke, M. (2005). Insect-Plant Biology. Oxford: Oxford University Press.
Shelomi, M., Perkins, L. E., Cribb, B. W., and Zalucki, M. P. (2010). Effects of leaf surfaces on first-instar Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) behaviour. Austr. J. Entomol. 49, 289–295. doi: 10.1111/j.1440-6055.2010.00766.x
Simmonds, A. T., and Gurr, G. M. (2005). Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agr. Forest Entomol. 8, 1–11. doi: 10.1111/j.1461-9563.2006.00271.x
Simmonds, A. T., Gurr, G. M., McGrath, D., Martin, P. M., and Nicol, H. I. (2004). Entrapment of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on glandular trichomes of Lycopersicon species. Austr. J. Entomol. 43, 196–200. doi: 10.1111/j.1440-6055.2004.00414.x
Stam, J. M., Kroes, A., Li, Y., Gols, R., van Loon, J. J., Poelman, E. H., et al. (2014). Plant interactions with multiple insect herbivores: From community to genes. Annu. Rev. Plant Biol. 65, 689–713. doi: 10.1146/annurev-arplant-050213-035937
Stamp, N. E., and Bowers, M. D. (1990). Body temperature, behavior, and growth of early-spring caterpillars (Hemileuca lucina: Saturniidae). J. Lepidopter. Soc. 44, 143–155.
Tian, D., Peiffer, M., Chung, S. H., and Felton, G. W. (2012). Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236, 1053–1066. doi: 10.1007/s00425-012-1651-9
Tsubaki, Y., and Shiotsu, Y. (1982). Group feeding as a strategy for exploiting food resources in the burnet moth Pryeria sinica. Oecologia 55, 12–20. doi: 10.1007/BF00386712
Vieira, C., and Romero, G. Q. (2013). Ecosystem engineers on plants: indirect facilitation of arthropod communities by leaf-rollers at different scales. Ecology 94, 1510–1518. doi: 10.1890/12-1151.1
Voigt, D., Gorb, E., and Gorb, S. (2007). Plant surface–bug interactions: Dicyphus errans stalking along trichomes. Arthropod. Plant Inter. 1:221. doi: 10.1007/s11829-007-9021-4
Ward, A., and Webster, M. (2016). Sociality: The Behaviour of Group-Living Animals. Springer. doi: 10.1007/978-3-319-28585-6
Weed, A. S. (2010). Benefits of larval group feeding by Chrysolina aurichalcea asclepiadis on vincetoxicum: improved host location or feeding facilitation? Entomol. Exp. Et Appl. 137, 220–338. doi: 10.1111/j.1570-7458.2010.01057.x
Will, T., Furch, A. C., and Zimmerman, M. R. (2013). How phloem-feeding insects face the challenge of phloem-located defenses. Front. Plant Sci. 4:336. doi: 10.3389/fpls.2013.00336
Young, A. (1983). On the evolution of egg placement and gregariousness of caterpillars in the Lepidoptera. Acta Biotheor. 32, 43–60. doi: 10.1007/BF00047974
Young, A. M., and Moffett, M. W. (1979a). Behavioral regulatory mechanisms in populations of the butterfly Mechanitis isthmia in Costa Rica: adaptations to host plants in secondary and agricultural habitats (Lepidoptera: Nymphalidae: Ithomiinae). Deutsc. Entomol. Zeitschr. 26, 21–38. doi: 10.1002/mmnd.4800260104
Young, A. M., and Moffett, M. W. (1979b). Studies on the population biology of the tropical butterfly Mechanitis isthmia in Costa Rica. Am. Midl. Natur. 101, 309–319. doi: 10.2307/2424596
Zalucki, M. P., Malcolm, S. B., Paine, T. D., Hanlon, C. C., Brower, L. P., and Clarke, A. R. (2001). It's the first bites that count: survival of first-instar monarchs on milkweeds. Austr. Ecol. 26, 547–555. doi: 10.1046/j.1442-9993.2001.01132.x
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