Skip to main content
Log in

Defensive responses by a social caterpillar are tailored to different predators and change with larval instar and group size

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Gregariousness in animals is widely accepted as a behavioral adaptation for protection from predation. However, predation risk and the effectiveness of a prey’s defense can be a function of several other factors, including predator species and prey size or age. The objective of this study was to determine if the gregarious habit of Malacosoma disstria caterpillars is advantageous against invertebrate natural enemies, and whether it is through dilution or cooperative defenses. We also examined the effects of larval growth and group size on the rate and success of attacks. Caterpillars of M. disstria responded with predator-specific behaviors, which led to increased survival. Evasive behaviors were used against stinkbugs, while thrashing by fourth instar caterpillars and holding on to the silk mat by second instar caterpillars was most efficient against spider attacks. Collective head flicking and biting by groups of both second and fourth instar caterpillars were observed when attacked by parasitoids. Increased larval size decreased the average number of attacks by spiders but increased the number of attacks by both stinkbugs and parasitoids. However, increased body size decreased the success rate of attacks by all three natural enemies and increased handling time for both predators. Larger group sizes did not influence the number of attacks from predators but increased the number of attacks and the number of successful attacks from parasitoids. In all cases, individual risk was lower in larger groups. Caterpillars showed collective defenses against parasitoids but not against the walking predators. These results show that caterpillars use different tactics against different natural enemies. Overall, these tactics are both more diverse and more effective in fourth instar than in second instar caterpillars, confirming that growth reduces predation risk. We also show that grouping benefits caterpillars through dilution of risk, and, in the case of parasitoids, through group defenses. The decreased tendency to aggregate in the last larval instar may therefore be linked to decreasing predation risk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Addy ND (1969) Rearing the forest tent caterpillar on an artificial diet. J Econ Entomol 62:270–271

    Google Scholar 

  • Benrey B, Denno RF (1997) The slow-growth–high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–999

    Google Scholar 

  • Botham MS, Kerfoot CJ, Louca V, Krause J (2005) Predator choice in the field; grouping guppies, Poecilia reticulata, receive more attacks. Behav Ecol Sociobiol 59:181–184

    Article  Google Scholar 

  • Botham MS, Kerfoot CJ, Louca V, Krause J (2006) The effects of different predator species on antipredator behavior in the Trinidadian guppy, Poecilia reticulata. Naturwissenschaften 93:431–439

    Article  PubMed  CAS  Google Scholar 

  • Castellanos I, Barbosa P (2006) Evaluation of predation risk by a caterpillar using substrate-borne vibrations. Anim Behav 72:461–469

    Article  Google Scholar 

  • Clark BR, Faeth SH (1997) The consequences of larval aggregation in the butterfly Chlosyne lacinia. Ecol Entomol 22:408–415

    Article  Google Scholar 

  • Cohen JE, Pimm SL, Yodzis P, Saldana J (1993) Body sizes of animal predators and animal prey in food webs. J Anim Ecol 62:67–78

    Article  Google Scholar 

  • Costa JT (1993) Larval ontogeny and survivorship of eastern tent caterpillar colonies. J Res Lepid 32:89–98

    Google Scholar 

  • De Clercq P, Wyckhuys K, De Oliveira HN, Klapwijk J (2002) Predation by Podisus maculiventris on different life stages of Nezara viridula. Fla Entomol 85:197–202

    Article  Google Scholar 

  • Despland E, Le Huu A (2007) Pros and cons of group-living in the forest tent caterpillar: separating the roles of silk and of grouping. Entomol Exp Appl 122(2):181–189

    Article  Google Scholar 

  • DeVito J (2003) Metamorphic synchrony and aggregation as antipredator responses in American toads. Oikos 103:75–80

    Article  Google Scholar 

  • Evans EW (1982) Influence of weather on predator/prey relations: stinkbugs and tent caterpillars. N Y Entomol Soc 4:241–246

    Google Scholar 

  • Evans EW (1983) Niche relations of predatory stinkbugs (Podisus spp., Pentatomidae) attacking tent caterpillars (Malacosoma americanum, Lasiocampidae). Am Midl Nat 109:316–323

    Article  Google Scholar 

  • Fitzgerald TD (1995) The tent caterpillars. Cornell University Press, Ithaca

    Google Scholar 

  • Fitzgerald TD, Costa JT (1999) Collective behavior in social caterpillars. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser, Basel

    Google Scholar 

  • Gaston KJ, Chown SL, Styles CV (1997) Changing size and changing enemies: the case of the mopane worm. Acta Oecol-Int J Ecol 18:21–26

    Article  Google Scholar 

  • Grisdale D (1985) Malacosoma disstria. In: Singh P, Moore RF (eds) Handbook of insect rearing. Elsevier, Amsterdam, pp 369–379

    Google Scholar 

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311

    Article  PubMed  CAS  Google Scholar 

  • Hass CC, Valenzuela D (2002) Anti-predator benefits of group living in white-nosed coatis (Nasua narica). Behav Ecol Sociobiol 51:570–578

    Article  Google Scholar 

  • Heinrich B (1983) Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64:592–602

    Article  Google Scholar 

  • Heinrich B (1993a) The hot blood insects: strategies and mechanisms of insect thermoregulation. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Heinrich B (1993b) How avian predators constrain caterpillar foraging. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman & Hall, New York, pp 224–248

    Google Scholar 

  • Hunter AF (2000) Gregariousness and repellent defences in the survival of phytophagous insects. Oikos 91:213–224

    Article  Google Scholar 

  • Iwao S, Wellington WG (1970) The western tent caterpillar: qualitative differences and the action of natural enemies. Res Popul Ecol XII:81–99

    Article  Google Scholar 

  • Krause J, Godin J-GJ (1995) Predator preferences for attacking particular group sizes: consequences for predator hunting success and prey predation risk. Anim Behav 50:465–473

    Article  Google Scholar 

  • Krause J, Reeves P, Hoare D (1998) Positioning behaviour in roach shoals: the role of body length and nutritional state. Behaviour 135:1031–1039

    Google Scholar 

  • Lawrence WS (1990) The effects of group size and host species on development and survivorship of a gregarious caterpillar Halisidota caryae (Lepidoptera: Arctiidae). Ecol Entomol 15:53–62

    Article  Google Scholar 

  • Lemos WP, Zanuncio JC, Serrao JE (2005) Attack behavior of Podisus rostralis (Heteroptera: Pentatomidade) adults on caterpillars of Bombyx mori (Lepidoptera: Bombycidae). Braz Arch Biol Technol 48:975–981

    Article  Google Scholar 

  • Levesque KR, Fortin M, Mauffette Y (2002) Temperature and food quality effects on growth, consumption and post-ingestive utilization efficiencies of the forest tent caterpillar Malacosoma disstria (Lepidoptera: Lasiocampidae). Bull Entomol Res 92:127–136

    Article  PubMed  CAS  Google Scholar 

  • McClure M, Despland E (2010) Collective foraging patterns of field colonies of Malacosoma disstria caterpillars. Can Entomol 142:1–8

    Article  Google Scholar 

  • McClure M, Cannell E, Despland E (2010) Thermal ecology and behaviour of the nomadic social forager. Malacosoma disstria. Phys Entomol. doi:10.1111/j.1365-3032.2010.00770.x

    Google Scholar 

  • Mooring MS, Hart BL (1992) Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behavior 123:173–193

    Article  Google Scholar 

  • Morris RF (1963) The effect of predator age and prey defense on the functional response of Podisus maculiventris Say to the density of Hyphantria cunea Drury. Can Entomol 95:1009–1023

    Article  Google Scholar 

  • Parry D, Spence JR, Volney WJA (1998) Budbreak phenology and natural enemies mediate survival of first-instar forest tent caterpillar (Lepidoptera: Lasiocampidae). Environ Entomol 27:1368–1374

    Google Scholar 

  • Peters RH (1983) The ecological implication of body size. Cambridge University Press, Cambridge

    Google Scholar 

  • Peterson SC, Johnson ND, LeGuyader JL (1987) Defensive regurgitation of allelochemicals derived from host cyanogenesis by eastern tent caterpillars. Ecology 68:1268–1272

    Article  Google Scholar 

  • Prop N (1960) Protection against birds and parasites in some species of tenthredinid larvae. Arch Néerl Zool 13:380–447

    Article  Google Scholar 

  • Reader T, Hochuli DF (2003) Understanding gregariousness in a larval Lepidoptera: the roles of host plant, predation, and microclimate. Ecol Entomol 28:729–737

    Article  Google Scholar 

  • Reavey D (1993) Why body size matters to caterpillars. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 248–279

    Google Scholar 

  • Rogovin K, Randall JA, Kolosova I, Moshkin M (2004) Predation on a social desert rodent, Rhombomys opimus: effect of group size, composition, and location. J Mammal 85:723–730

    Article  Google Scholar 

  • Ronnas C, Larsson S, Pitacco A, Battisti A (2010) Effects of colony size on larval performance in a processionary moth. Ecol Entomol 35:436–445

    Google Scholar 

  • Schultz JC (1983) Habitat selection and foraging tactics of caterpillars in heterogeneous trees. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 61–90

    Google Scholar 

  • Seyfarth RM, Cheney DL, Marler P (1980) Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science 210:801–803

    Article  PubMed  CAS  Google Scholar 

  • Smith GR, Awan AR (2009) The roles of predator identity and group size in the antipredator responses of American toad (Bufo americanus) and bullfrog (Rana catesbeiana) tadpoles. Behaviour 146:225–243

    Article  Google Scholar 

  • Tostowaryk W (1971) Relationship between parasitism and predation in diprionid sawflies. Ann Entomol Soc Am 64:1424–1427

    Google Scholar 

  • Uetz GW, Boyle J, Hieber CS, Wilcox SR (2002) Antipredator benefits of group living in colonial web-building spiders: the 'early warning' effect. Anim Behav 63:445–452

    Article  Google Scholar 

  • Vulinec K (1990) Collective security: aggregation by insects as a defense. In: Evans DL, Schmidt JO (eds) Insect defenses. Adaptive mechanisms of prey and predators. State University of New York, Albany, New York, pp 251–288

    Google Scholar 

  • Wajnberg E (2006) Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms. Behav Ecol Sociobiol 60:589–611

    Article  Google Scholar 

  • Warren PH, Lawton JH (1987) Invertebrate predator–prey body size relationships: an explanation for upper triangular food webs and patterns in food web structure? Oecologia 74:231–235

    Article  Google Scholar 

  • Webb JK, Du W, Pike D, Shine R (2010) Generalization of predator recognition: velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes. Curr Zool 56:337–342

    Google Scholar 

  • Williams DJM, Parry D and Langor DW (1996) Sampling and identification of forest tent caterpillar parasitoids in the Prairie Provinces. Canadian Forest Service NR, Northern Forestry Centre:Information Report NOR-X-345

Download references

Acknowledgments

Thanks go to Dr. Don Stoltz (Dalhousie Univeristy in Halifax, Canada) for providing the facilities and insects to complete the parasitoid experiments. Experiments done at Dalhousie were possible due to financial assistance by Dr. Stoltz and a travel scholarship to MM awarded by Centre d’Étude de la Forêt. Financial support was provided by the Canadian Natural Sciences and Engineering Research Council as a Discovery Grant to ED, and by a Canadian Natural Sciences and Engineering Research Council Graduate Student Research Award to MM. The experiments comply with the current laws of the country in which they were performed.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emma Despland.

Additional information

Communicated by Sven Thatje

Rights and permissions

Reprints and permissions

About this article

Cite this article

McClure, M., Despland, E. Defensive responses by a social caterpillar are tailored to different predators and change with larval instar and group size. Naturwissenschaften 98, 425–434 (2011). https://doi.org/10.1007/s00114-011-0788-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-011-0788-x

Keywords

Navigation