Abstract
Chemical defences against predation often involve responses to specific predation events where the prey expels fluids, such as haemolymph or gut contents, which are aversive to the predator. The common link is that each predation attempt that is averted results in an energetic cost and a reduction in the chemical defences of the prey, which might leave the prey vulnerable if the next predation attempt occurs soon afterwards. Since prey appear to be able to control the magnitude of their responses, we should expect them to trade-off the need to repel the current threat against the need to preserve defences against future threats and conserve energy for other essential activities. Here we use dynamic state-dependent models to predict optimal strategies of defence deployment in the juvenile stage of an animal that has to survive to maturation. We explore the importance of resource level, predator density, and the costs of making defences on the magnitude of the responses and optimal age and size at maturation. We predict the patterns of investment and the magnitude of the deployment of defences to potentially multiple attacks over the juvenile period, and show that responses should be smaller when the costs of defences and/or predation risk are higher. The model enables us to predict that animals in which defences benefit the adult stage will employ different strategies than those that do not use the same defences as adults, and thereby experience a smaller reduction in body size as a result of repeated attacks. We also explore the effect of the importance of adult size, and find that the sex and mating system of the prey should also affect defensive strategies. Our work provides the first predictive theory of the adaptive use of responsive defences across taxa.
Similar content being viewed by others
References
Amano T, Nishida R, Kuwahara Y, Fukami H (1999) Pharmocophagous acquisition of clerodendrins by the turnip sawfly (Athalia rosaw ruficornis) and their role in the mating behavior. Chemoecology 9:145–150
Arendt JD (1997) Adaptive variation in growth rates: an integration across taxa. Q Rev Biol 72:149–177
Banks MJ, Thompson DJ (1987) Lifetime reproductive success of females of the damselfly Coenagrion puella. J Anim Ecol 56:815–832
Blakley N (1981) Life history significance of size-triggered metamorphosis in milkweed bugs (Oncopeltus). Ecology 62:57–64
Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407
Blum MS (1981) Chemical defenses of arthropods. Academic Press, London
Boevé J, Müller C (2005) Defence effectiveness of easy bleeding sawfly larvae towards invertebrate and avian predators. Chemoecology 15:51–58
Boevé J, Schaffner U (2003) Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis. Oecologia 134:104–111
Brower LP (1984) Chemical defence in butterflies. In: Vane-Wright RI, Ackery P (eds) The biology of butterflies. Princeton University Press, Princeton, pp 109–134
Bowers MD (1992) The evolution of unpalatability and the cost of chemical defense in insects. In: Evans DL, Schmidt JO (eds) Insect chemical ecology. Chapman & Hall, London, pp 216–244
Bowers MD (1993) Aposematic caterpillars: life-styles of the warningly colored and unpalatable. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman & Hall, London, pp 331–371
Caro TM (2005) Antipredator defenses in birds and mammals. University of Chicago, Chicago
Clark CW, Mangel M (2000) Dynamic state variable models in ecology. Oxford University Press, Oxford, UK
Cohen JA (1985) Differences and similarities in cardenolide contents of queen and monarch butterflies in Florida and their ecological and evolutionary implications. J Chem Ecol 11:85–103
Coley PD, Bateman ML, Kursar TA (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228
Davidowitz G, D’Amico LJ, Nijhout HF (2004) The effects of environmental variation on a mechanism that controls insect body size. Evol Ecol Res 6:49–62
de Jong PW, Holloway GJ, Brakefield PM, de Vos H (1991) Chemical defence in ladybird beetles (Coccinellidae). II. Amount of reflex fluid, the alkaloid adaline and individual variation in defence in 2-spot ladybirds (Adalia bipunctata). Chemoecology 2:15–19
del Campo ML, Smedley SR, Eisner T (2005) Reproductive benefits derived from defensive plant alkaloid possession in an arctiid moth (Utethesia ornatrix). Proc Natl Acad Sci USA 102:13508–13512
Derby CD (2007) Escape by inking and secreting: marine molluscs avoid predators through a rich array of chemicals and mechanisms. Biol Bull 213:274–289
Eisner T (1958) The protective role of the spray mechanism of the bombadier beetle, Brachynus ballistarius. J Insect Physiol 2:215–220
Eisner T, Rossini C, González A, Eisner M (2004) Chemical defense of an opilionid (Acanthopachylus aculeatus). J Exp Biol 207:1313–1321
Eisner T, Eisner M, Aneshansley D (2005) Pre-ingestive treatment of bombadier beetles by jays: food preparation by “anting” and “sand-wiping”. Chemoecology 15:227–233
Etilé E, Despland E (2008) Developmental variation in the forest tent caterpillar: life history consequences of a threshold size for pupation. Oikos 117:135–143
Gentry GL, Dyer LA (2002) On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology 83:3108–3119
Grant JB (2006) Diversification of gut morphology in caterpillars is associated with defensive behavior. J Exp Biol 209:3018–3024
Grill CP, Moore AJ (1998) Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle. Oecologia 114:274–282
Hartmann T, Theuring C, Beuerle T, Bernays EA (2004) Phenological fate of plant-acquired pyrrolizidine alkaloids in the polyphagous arctiid Estigmene acrea. Chemoecology 14:207–216
Holloway GJ, de Jong PW, Brakefield PM, de Vos H (1991) Chemical defence in ladybird beetles (Coccinellidae). 1. Distribution of coccinelline and individual variation in defence in 7-spot ladybirds (Coccinella septempunctata). Chemoecology 2:7–14
Järvi T, Sillèn-Tullberg B, Wiklund C (1981) The cost of being aposematic—an experimental study of predation on larvae of Papilio machaon by the great tit, Parus major. Oikos 36:267–272
Labeyrie E, Blanckenhorn WU, Rahier M (2003) Mate choice and toxicity in two species of leaf beetles with different types of chemical defence. J Chem Ecol 29:1665–1680
Leather SR (1988) Size, reproductive potential and fecundity in insects: things aren’t as simple as they seem. Oikos 51:386–389
Moore KA, Williams DD (1990) Novel strategies in the complex defense repertoire of a stonefly (Pteronarcys dorsata) nymph. Oikos 57:49–56
Müller C, Brakefield PM (2003) Analysis of a chemical defense in sawfly larvae: easy bleeding targets predatory wasps in late summer. J Chem Ecol 29:2683–2694
Müller C, Agerbirk N, Olsen CE, Boevé J, Schaffner U, Brakefield PM (2001) Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J Chem Ecol 27:2505–2516
Nishida R, Fukami H (1990) Sequestration of distasteful compounds by some pharmocophagous insects. J Chem Ecol 16:151–164
Pasteels JM, Grégoire JC, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Annu Rev Entomol 28:263–289
Pasteels JM, Theuring C, Witte L, Hartmann T (2003) Sequestration and metabolism of protoxic pyrrolizidine alkaloids by larvae of the leaf beetle Platyphora boucardi and their transfer via pupae into defensive secretions of adults. J Chem Ecol 29:337–355
Peck DC (2000) Reflex bleeding in froghoppers (Homoptera: Cercopidae): Variation in behavior and taxomonic distribution. Ann Entomol Soc Am 93:1186–1194
Peters RH (1983) Ecological implications of body size. Cambridge University Press, Cambridge
Peterson SC, Johnson ND, LeGuyader JL (1987) Defensive regurgitation of allelochemicals derived from host cyanogenesis by eastern tent caterpillars. Ecology 68:1268–1272
Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. Oxford University Press, Oxford
Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192
Sillen-Tullberg B, Leimar O (1988) The evolution of gregariousness in distasteful insects as a defence against predators. Am Nat 132:723–734
Sokolovska N, Rowe L, Johansson F (2000) Fitness and body size in mature odonates. Ecol Entomol 25:239–248
Tammaru T, Esperk T (2007) Growth allometry of immature insects: larvae do not grow exponentially. Funct Ecol 21:1099–1105
Taylor BW, Anderston CR, Peckarsky B (1998) Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success. Oecologia 114:494–502
Vlieger L, Brakefield PM, Muller C (2004) Effectiveness of the defence mechanism of the turnip sawfly, Athalia rosae (Hymenoptera: Tenthredinidae), against predation by lizards. Bull Entomol Res 94:283–289
Whitman DW, Blum MS, Alsop DW (1990) Allomones: chemicals for defense. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, New York, pp 229–251
Wiklund C, Järvi T (1982) Survival of distasteful insects after being attacked by naive birds: a reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution 36:998–1002
Zalucki MP, Brower LP, Alonso A (2001) Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecol Entomol 26:212–224
Acknowledgements
This manuscript benefited from critical readings by Tom Sherratt, John Skelhorn, Mike Speed and two anonymous referees. A. D. H. was supported by NERC grants NE/E016626/1 awarded to G. D. R. and NE/E018521/1 awarded to Mike Speed. G. D. R. is also supported by NERC grants NE/F002653/1, NE/D010500/1 and NE/D010772/1.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Wolf Mooij.
Rights and permissions
About this article
Cite this article
Higginson, A.D., Ruxton, G.D. Dynamic state-dependent modelling predicts optimal usage patterns of responsive defences. Oecologia 160, 399–410 (2009). https://doi.org/10.1007/s00442-009-1296-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-009-1296-y