Abstract
Insect larvae increase in size with several orders of magnitude throughout development making them more conspicuous to visually hunting predators. This change in predation pressure is likely to impose selection on larval anti-predator behaviour and since the risk of detection is likely to decrease in darkness, the night may offer safer foraging opportunities to large individuals. However, forsaking day foraging reduces development rate and could be extra costly if prey are subjected to seasonal time stress. Here we test if size-dependent risk and time constraints on feeding affect the foraging–predation risk trade-off expressed by the use of the diurnal–nocturnal period. We exposed larvae of one seasonal and one non-seasonal butterfly to different levels of seasonal time stress and time for diurnal–nocturnal feeding by rearing them in two photoperiods. In both species, diurnal foraging ceased at large sizes while nocturnal foraging remained constant or increased, thus larvae showed ontogenetic shifts in behaviour. Short night lengths forced small individuals to take higher risks and forage more during daytime, postponing the shift to strict night foraging to later on in development. In the non-seasonal species, seasonal time stress had a small effect on development and the diurnal–nocturnal foraging mode. In contrast, in the seasonal species, time for pupation and the timing of the foraging shift were strongly affected. We argue that a large part of the observed variation in larval diurnal–nocturnal activity and resulting growth rates is explained by changes in the cost/benefit ratio of foraging mediated by size-dependent predation and time stress.
Similar content being viewed by others
References
Abrams PA, Leimar O, Nylin S, Wiklund C (1996) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. Am Nat 147:381–395
Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Tree 18:234–240
Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177
Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Tree 12:235–239
Atlegrim O (1992) Mechanisms regulating bird predation on a herbivorous larva guild in boreal coniferous forests. Ecography 15:19–24
Baker RL, Ball SL (1995) Microhabitat selection by larval Chironomus tentans (Diptera, Chironomidae)—effects of predators, food, cover and light. Freshw Biol 34:101–106
Berger D, Walters R, Gotthard K (2006) What keeps insects small?—size dependent predation on two species of butterfly larvae. Evol Ecol 20:575–589
Bradford MJ, Higgins PS (2001) Habitat-, season-, and size-specific variation in diel activity patterns of juvenile chinook salmon (Oncorhynchus tshawytscha) and steelhead trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 58:365–374
Buckner CH (1966) The role of vertebrate predators in the biological control of forest insects. Ann Rev Entomol 11:449–470
Casey TM (1993) Effects of temperature on foraging of caterpillars. In: Stamp NE, Casey TM (eds) Caterpillars—ecological and evolutionary constraints on foraging, chapter 1. Chapman & Hall, New York, pp 5–28
Clark CW (1994) Antipredator behavior and the asset-protection principle. Behav Ecol 5:159–170
Culp JM, Scrimgeour GJ (1993) Size-dependent diel foraging periodicity of a mayfly grazer in streams with and without fish. Oikos 68:242–250
D’Amico LJ, Davidowitz G, Nijhout HF (2001) The development and physiological basis of body size evolution in an insect. Proc R Soc Lond B 268:1589–1593
Dempster JP (1984) The natural enemies of butterflies. In: Vane-Wright RI, Ackery PR (eds) The Biology of Butterflies. Academic, London, pp 97–104
Eliasson CU, Ryrholm N, Holmer M, Jilg K, Gärdenfors U (2005) Nationalnyckeln till Sveriges flora och fauna. Fjärilar: Dagfjärilar. Hesperidae–Nymphalidae. Reuter Media Group, ArtDatabanken, SLU, Uppsala. Laholm, Sweden
Esperk T (2006) Larval instar as a key element of insect growth schedules. PhD thesis, Tartu University, Tartu, Estonia
Feeny P, Blau WS, Kareiva PM (1985) Larval growth and survivorship of the black swallowtail butterfly in central New York. Ecol Monogr 55:167–187
Fraser DF, Gilliam JF, Akkara JT, Albanese BW, Snider SB (2004) Night feeding by guppies under predator release: effects on growth and daytime courtship. Ecology 85:312–319
Gilliam JF, Fraser DF (1987) Habitat selection under predation hazard—test of a model with foraging minnows. Ecology 68:1856–1862
Gotthard K (2001) Growth strategies of ectothermic animals in temperate environments. In: Atkinson D, Thorndyke M (eds) Animal developmental ecology. BIOS Scientific, Oxford
Hassell MP, Southwood TRE (1978) Foraging strategies of insects. Ann Rev Ecolog Syst 9:75–98
Heinrich B (1993) How avian predators constrain caterpillar foraging. In: Stamp NE, Casey TM (eds) Caterpillars—ecological and evolutionary constraints on foraging, chapter 7. Chapman & Hall, New York, pp 224–247
Houston A, Clark C, McNamara J, Mangel M (1988) Dynamic models in behavioral and evolutionary ecology. Nature 332:29–34
Imre I, Boisclair D (2004) Age effects on diel activity patterns of juvenile Atlantic salmon: parr are more nocturnal than young-of-the-year. J Fish Biol 64:1731–1736
Johansson F, Rowe L (1999) Life history and behavioral responses to time constraints in a damselfly. Ecology 80:1242–1252
Johansson F, Stoks R, Rowe L, De Block M (2001) Life history plasticity in a damselfly: effects of combined time and biotic constraints. Ecology 82:1857–1869
Kingsolver JG, Ragland GJ, Shlichta JG (2004) Quantitative genetics of continuous reaction norms: thermal sensitivity of caterpillar growth rates. Evolution 58:1521–1529
Kingsolver JG, Woods HA (1997) Thermal sensitivity of growth and feeding in Manduca sexta caterpillars. Physiol Biochem Zool 70:631–638
Koops MA, Abrahams MV (1998) Life history and the fitness consequences of imperfect information. Evol Ecol 12:601–613
Kozlowski J (1992) Optimal allocation of resources to growth and reproduction—implications for age and size at maturity. Tree 7:15–19
Kristensen CO (1994) Investigations on the natural mortality of eggs and larvae of the large white Pieris brassicae (Lep-Pieridae). J Appl Entomol 117:92–98
Krivan V, Vrkoc I (2000) Patch choice under predation hazard. Theor Popul Biol 58:329–340
Kronfeld-Schor N, Dayan T (2003) Partitioning of time as an ecological resource. Ann Rev Ecol Evol Syst 34:153–181
Lampert W (1989) The adaptive significance of diel vertical migration of zooplankton. Func Ecol 3:21–27
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:549–659
Ludwig D, Rowe L (1990) Life-history strategies for energy gain and predator avoidance under time constraints. Am Nat 135:686–707
Macchiusi F, Baker RL (1992) Effects of predators and food availability on activity and growth of Chironomus tentans (Chironomidae, Diptera). Freshw Biol 28:207–216
Metcalfe NB, Fraser NHC, Burns MD (1998) State-dependent shifts between nocturnal and diurnal activity in salmon. Proc R Soc Lond B 265:1503–1507
Metcalfe NB, Fraser NHC, Burns MD (1999) Food availability and the nocturnal vs. diurnal foraging trade-off in juvenile salmon. J Anim Ecol 68:371–381
Montllor CB, Bernays EA (1993) Invertebrate predators and caterpillar foraging. In: Stamp NE, Casey TM (eds) Caterpillars—ecological and evolutionary constraints on foraging, chapter 5. Chapman & Hall, New York, pp 170–203
Nylin S, Gotthard K (1998) Plasticity in life-history traits. Ann Rev Entomol 43:63–83
Nylin S, Wickman PO, Wiklund C (1989) Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae). Biol J Linn Soc 38:155–171
Park O (1940) Nocturnalism—the development of a problem. Ecol Monogr 10:485–536
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge, Cambridge University Press
Reavey D (1993) Why body size matters to caterpillars. In: Stamp NE, Casey TM (eds) Caterpillars—ecological and evolutionary constraints on foraging, chapter 8. Chapman & Hall, New York, pp 248–282
Roff DA (2002) Life history evolution. Sinnauer, Sunderland, USA
Sibly RM, Calow P, Nichols N (1985) Are patterns of growth adaptive? J Theor Biol 112:553–574
Sih A, Ziemba R, Harding KC (2000) New insights on how temporal variation in predation risk shapes prey behavior. Tree 15:3–4
Slansky F (1993) Nutritional ecology: the fundamental quest for nutrients. In: Stamp NE, Casey TM (eds) Caterpillars—ecological and evolutionary constraints on foraging, chapter 2. Chapman & Hall, New York, pp 29–92
Stamp NE, Bowers D (1990) Variation in food quality and temperature constrain foraging of gregarious caterpillars. Ecology 71:1031–1039
Stamp NE, Wilkens RT (1993) On the cryptic side of life: being unapparent to enemies and the consequences for foraging and growth in caterpillars. In: Stamp NE, Casey TM (eds) Caterpillars—ecological and evolutionary constraints on foraging, chapter 9. Chapman & Hall, New York, pp 283–331
Takeda M (2005) Differentiation in life cycle of sympatric populations of two forms of Hypantria moth in central Missouri. Entomol Sci 8:211–218
Tikkanen P, Muotka T, Huhta A (1994) Predator detection and avoidance by lotic mayfly nymphs of different size. Oecologia 99:252–259
Tolman T (1997) Butterflies of Europe. Princeton University Press, Princeton
Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality-rates mediated by foraging activity. Am Nat 142:242–272
Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Ann Rev Ecolog Syst 15:393–425
Wickman P-O, Wiklund C, Karlsson B (1990) Comparative phenology of four satyrine butterflies inhabiting dry grasslands in Sweden. Hol Ecol 13:238–346
Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behaviour of first instar larval Lepidoptera. Ann Rev Entomol 47:361–393
Acknowledgements
We would like to thank C. Wiklund, C. Stefanescu and N. Metcalfe for valuable comments on the manuscript. We are also grateful to the young and talented students of the Stockholm Research School that helped in collecting data on behaviour. This study has been performed in agreement with the Swedish current laws and regulations and was funded by grants from the Swedish Research Council and Formas to K.G.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by T. Moore
Rights and permissions
About this article
Cite this article
Berger, D., Gotthard, K. Time stress, predation risk and diurnal–nocturnal foraging trade-offs in larval prey. Behav Ecol Sociobiol 62, 1655–1663 (2008). https://doi.org/10.1007/s00265-008-0594-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-008-0594-4