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Nymphal density, behavioral development, and life history in a field cricket

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Abstract

Population density regulates the strength of intraspecific competition and may thereby be reflected in life-history variables, such as development time, growth rate, or investment in immune defense. However, population density may also affect the fitness payoffs of different behaviors and consequently shape the development of personality. Here we studied if population density during nymphal development (one, four, or ten individuals raised together) affects the level of boldness, measured as the latency time to recover from freezing and emerge from a shelter, aggressiveness towards conspecifics or their correlation at the adult stage in the field crickets, Gryllus integer. In addition, we tested if individuals invest more resources in immune function or speed up their development in response to a high conspecifics density during ontogeny. Nymphal density did not affect adult boldness or aggressiveness towards conspecific males per se, but these variables showed a negative association, i.e., indicated an unconventional behavioral syndrome in the highest density treatment. Supporting the effectiveness of density treatments in inducing plastic responses, individuals reached maturity sooner and invested more resources in immune function in the highest nymphal density group compared to groups consisting of one or four individuals. Our results suggest that population density may play an important role in shaping both the realized life history and development of behavioral syndromes.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophot Int 11:36–42

    Google Scholar 

  • Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 34:517–547

    Article  Google Scholar 

  • Anand AN, Lorenz MW (2008) Age-dependent changes of fat body stores and the regulation of fat body lipid synthesis and mobilisation by adipokinetic hormone in the last larval instar of the cricket, Gryllus bimaculatus. J Insect Physiol 54:1404–1412

    Article  PubMed  CAS  Google Scholar 

  • Applebaum SW, Heifetz Y (1999) Density-dependent physiological phase in insects. Annu Rev Entomol 44:317–341

    Article  PubMed  CAS  Google Scholar 

  • Armitage SAO, Thompson JJW, Rolff J, Siva-Jothy MT (2003) Examining costs of induced and constitutive immune investment in Tenebrio molitor. J Evol Biol 16:1038–1044

    Article  PubMed  CAS  Google Scholar 

  • Arneberg P, Skorping A, Grenfell B, Read AF (1998) Host densities as determinants of abundance in parasite communities. Proc R Soc Lond B 266:1283–1289

    Article  Google Scholar 

  • Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond B 277:503–511

    Article  Google Scholar 

  • Baldal EA, van der Linde K, van Alpen JJM, Brakefield PM, Zwaan BJ (2005) The effects of larval density on adult life-history traits in three species of Drosophila. Mech Ageing Dev 126:407–416

    Article  PubMed  CAS  Google Scholar 

  • Barber I, Dingemanse NJ (2010) Parasitism and the evolutionary ecology of animal personality. Phil Trans R Soc Lond B 365:4077–4088

    Article  Google Scholar 

  • Barnes AI, Siva-Jothy MT (2000) Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanisation is an indicator of investment in immunity. Proc R Soc Lond B 267:177–182

    Article  CAS  Google Scholar 

  • Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834

    Article  PubMed  Google Scholar 

  • Box GEB, Cox DR (1964) An analysis of transformations. J R Stat Soc B Met 26:211–252

    Google Scholar 

  • Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510

    Article  PubMed  CAS  Google Scholar 

  • Chelini M-C, Willemart RH, Hebets EA (2009) Costs and benefits of freezing behaviour in the harvestman Eumososoma roeweri (Arachnida, Opilioides). Behav Process 82:153–159

    Article  Google Scholar 

  • Cote I, Poulin R (1995) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159–165

    Article  Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  PubMed  CAS  Google Scholar 

  • Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Phil Trans R Soc Lond B 365:3947–3958

    Article  Google Scholar 

  • Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138

    Article  PubMed  Google Scholar 

  • Dingle H (1996) Migration: the biology of life on the move. Oxford University Press, Oxford

    Google Scholar 

  • Dingle H, Winchell R (1997) Juvenile hormone as a mediator of plasticity in insect life histories. Arch Insect Biochem Physiol 35:359–373

    Article  CAS  Google Scholar 

  • Ernande B, Dieckmann U (2004) The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics. J Evol Biol 17:613–628

    Article  PubMed  CAS  Google Scholar 

  • Freitak D, Ots I, Horak P (2003) Immune response in energetically costly in white cabbage butterfly pupae. Proc R Soc Lond B 270:220–222

    Article  Google Scholar 

  • Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643

    Article  PubMed  CAS  Google Scholar 

  • Goodbrod JR, Goff ML (1990) Effects of larval population density on rates of development and interactions between two species of Chrysomya (Diptera: Calliphoridae) in laboratory culture. J Med Entomol 27:338–343

    PubMed  CAS  Google Scholar 

  • Goulson D, Cory JS (1995) Responses of Mamestra brassicae (Lepidoptera: Noctuidae) to crowding: interactions with disease resistance, colour phase and growth. Oecologia 104:416–423

    Article  Google Scholar 

  • Gyuris E, Feró O, Tartally A, Barta Z (2010) Individual behavior in firebugs (Pyrrhocoris apterus). Proc R Soc Lond B 278:628–633

    Article  Google Scholar 

  • Hedrick AV (2000) Crickets with extravagant mating songs compensate for predation risk with extra caution. Proc R Soc Lond B 267:671–675

    Article  CAS  Google Scholar 

  • Hedrick AV, Kortet R (2006) Hiding behaviour in two cricket populations that differ in predation pressure. Anim Behav 72:1111–1118

    Article  Google Scholar 

  • Heifetz Y, Applebaum SW (1995) Density-dependent physiological phase in non-migratory grasshopper, Aiolopus thalassinus thalassinus. Entomol Exp Appl 77:251–262

    Article  Google Scholar 

  • Heino M, Kaitala V (1999) Evolution of resource allocation between growth and reproduction in animals with indeterminate growth. J Evol Biol 12:423–429

    Article  Google Scholar 

  • Hooper HL, Sibly RM, Hutchinson TH, Maund SJ (2003) The influence of larval density, food availability and habitat longevity on the life-history and population growth rate of the midge Chironomus riparius. Oikos 102:515–524

    Article  Google Scholar 

  • Iba M, Nagao T, Urano A (1995) Effects of population density on growth, behavior and levels of biogenic amines in the cricket, Gryllus bimaculatus. Zool Sci 12:695–702

    Article  CAS  Google Scholar 

  • Injeyan HS, Tobe SS (1981) Phase polymorphism in Schistocerca gregaria: reproductive parameters. J Insect Physiol 27:97–102

    Article  Google Scholar 

  • Jacot A, Scheuber H, Brinkhof WG (2004) Cost of an induced immune response on sexual display and longevity in field crickets. Evolution 58:2280–2286

    PubMed  Google Scholar 

  • Javois J, Tammaru T, Käär M (2005) Oviposition in an eruptive moth species, Yponomeuta evonymellus, is insensitive to the population density experienced during the larval period. Entomol Exp Appl 115:379–386

    Article  Google Scholar 

  • Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer-Verlak, New York

    Google Scholar 

  • Kortet R, Hedrick AV (2007) A behavioural syndrome in the field cricket Gryllus integer: intrasexual aggression is correlated with activity in a novel environment. Biol J Linn Soc 91:475–482

    Article  Google Scholar 

  • Kortet R, Rantala MJ, Hedrick A (2007) Boldness in anti-predator behaviour and immune defence in field crickets. Evol Ecol Res 9:185–197

    Google Scholar 

  • Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458

    Article  PubMed  Google Scholar 

  • Kraaijeveld AR, Godfray HCJ (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–280

    Article  PubMed  CAS  Google Scholar 

  • Kraaijeveld AR, Limentani EC, Godfray HC (2001) Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc R Soc Lond B 268:259–261

    Article  CAS  Google Scholar 

  • Lihoreau M, Rivault C (2008) Tactile stimuli trigger group effects in cockroach aggregations. Anim Behav 75:1965–1970

    Article  Google Scholar 

  • Lihoreau M, Brepson L, Rivault C (2009) The weight of the clan: even in insects, social isolation can induce a behavioural syndrome. Behav Process 82:81–84

    Article  Google Scholar 

  • Mangel M, Munch SB (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:155–176

    Article  Google Scholar 

  • Moret Y, Siva-Jothy MT (2003) Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc R Soc Lond B 270:2475–2480

    Article  CAS  Google Scholar 

  • Mueller LD, Guo P, Ayala FJ (1991) Density-dependent natural selection and trade-offs in life history traits. Science 253:433–435

    Article  PubMed  CAS  Google Scholar 

  • Paille N, Sainte-Marie B, Brethes J-C (2002) Behaviour, growth and survival of stage V lobsters (Homarus americanus) in relation to shelter availability and lobster density. Mar Freshw Behav Physiol 35:203–219

    Article  Google Scholar 

  • Ranta E, Lindström K (1993) Body size and shelter possession in mature signal crayfish, Pacifastacus leniusculus. Ann Zool Fenn 30:125–132

    Google Scholar 

  • Rantala MJ, Kortet R (2004) Male dominance and immunocompetence in the field cricket (Gryllus bimaculatus). Behav Ecol 15:187–191

    Article  Google Scholar 

  • Rantala MJ, Roff DA (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Funct Ecol 19:323–330

    Article  Google Scholar 

  • Reale D, Dingemanse NJ, Kazem AJN, Wright J (2010a) Evolutionary and ecological approaches to the study of personality. Phil Trans R Soc Lond B 365:3937–3946

    Article  Google Scholar 

  • Reale D, Garant D, Humbries MM, Bergeron P, Careau V, Montiglio P-E (2010b) Personality and the emergence of the pace-of-life syndrome concept at the population level. Phil Trans R Soc Lond B 365:4051–4063

    Article  Google Scholar 

  • Reeson AF, Wilson K, Gunn A, Hails RS, Goulson D (1998) Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density. Proc R Soc Lond B 265:1787–1791

    Article  Google Scholar 

  • Schmid-Hempel PS (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366

    Article  Google Scholar 

  • Schmid-Hempel PS (2005) Evolutionary ecology of insect immune defences. Annu Rev Entomol 50:529–551

    Article  PubMed  CAS  Google Scholar 

  • Schwartz A, Koella JC (2004) The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on immune activation. J Evol Biol 17:834–840

    Article  PubMed  CAS  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Stamps JA (2007) Growth-mortality trade-offs and ‛personality traits’ in animals. Ecol Lett 10:355–363

    Article  PubMed  Google Scholar 

  • Stamps JA, Groothuis GG (2010) Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Phil Trans R Soc Lond B 365:4029–4041

    Article  Google Scholar 

  • Tammaru T, Ruohomäki K, Montola M (2000) Crowding-induced plasticity in Epirrita autumnata (Lepidoptera: Geometridae): weak evidence of specific modifications in reaction norms. Oikos 90:171–181

    Article  Google Scholar 

  • Tanner CJ (2008) Chill out: cooling promotes aggressive behavior in the ant Formica xerophila. Insect Soc 56:64–69

    Article  Google Scholar 

  • Vainikka A, Rantala MJ, Niemelä P, Hirvonen H, Kortet R (2011) Boldness as a consistent personality trait in the noble crayfish, Astacus astacus. Acta Ethol 14:17–25

    Article  Google Scholar 

  • Weaver DK, McFarlane JE (1990) The effect of larval density on growth and development of Tenebrio molitor. J Insect Physiol 35:531–536

    Article  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Wilson K, Reeson AF (1998) Density-dependent prophylaxis: evidence from Lepidoptera–baculovirus interactions? Ecol Entomol 23:100–101

    Article  Google Scholar 

  • Wilson K, Cotter SC, Reeson AF, Pell JK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649

    Article  Google Scholar 

  • Wilson K, Thomas MB, Blanford S, Doggett M, Simpson SJ, Moore SL (2002) Coping with crowds: density-dependent disease resistance in desert locusts. Proc Natl Acad Sci U S A 8:5471–5475

    Article  Google Scholar 

  • Wilson K, Knell R, Boots M, Koch-Osborne J (2003) Group living and investment in immune defence: an interspecific analysis. J Anim Ecol 72:133–143

    Article  Google Scholar 

  • Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Phil Trans R Soc Lond B 365:3959–3968

    Article  Google Scholar 

  • Woodhead AP, Paulson CR (1983) Larval development of Diploptera punctata reared alone and in groups. J Insect Physiol 29:665–668

    Article  Google Scholar 

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Acknowledgments

This research has been supported by the Academy of Finland (project 127398). We would like to thank Arja Kaitala, Eija Hurme, Jukka Forsman, Sami Kivelä, Tatiana Czeschlik, Toomas Tammaru, all the members from the “round table” group, and one anonymous referee for valuable comments for earlier versions of the manuscript. We would also like to thank the University of Oulu Zoo and its very helpful staff for the help with experiments and maintenance of our cricket population. We thank also Annie Leonard, Ann Hedrick, and Markus Rantala who helped us to establish the laboratory population used in this study.

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The authors declare that they have no conflict of interest. All the experiment was conducted according to the Finnish legislation of animal care.

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Correspondence to Petri T. Niemelä.

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Communicated by M. Siva-Jothy

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Niemelä, P.T., Vainikka, A., Lahdenperä, S. et al. Nymphal density, behavioral development, and life history in a field cricket. Behav Ecol Sociobiol 66, 645–652 (2012). https://doi.org/10.1007/s00265-011-1312-1

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