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Oecologia

, Volume 144, Issue 3, pp 353–361 | Cite as

Larval food limitation in butterflies: effects on adult resource allocation and fitness

  • Carol L. Boggs
  • Kimberly D. Freeman
Ecophysiology

Abstract

Allocation of larval food resources affects adult morphology and fitness in holometabolous insects. Here we explore the effects on adult morphology and female fitness of larval semi-starvation in the butterfly Speyeria mormonia. Using a split-brood design, food intake was reduced by approximately half during the last half of the last larval instar. Body mass and forewing length of resulting adults were smaller than those of control animals. Feeding treatment significantly altered the allometric relationship between mass and wing length for females but not males, such that body mass increased more steeply with wing length in stressed insects as compared to control insects. This may result in changes in female flight performance and cost. With regard to adult life history traits, male feeding treatment or mating number had no effect on female fecundity or survival, in agreement with expectations for this species. Potential fecundity decreased with decreasing body mass and relative fat content, but there was no independent effect of larval feeding treatment. Realized fecundity decreased with decreasing adult survival, and was not affected by body mass or larval feeding treatment. Adult survival was lower in insects subjected to larval semi-starvation, with no effect of body mass. In contrast, previous laboratory studies on adult nectar restriction showed that adult survival was not affected by such stress, whereas fecundity was reduced in direct 11 proportion to the reduction of adult food. We thus see a direct impact of larval dietary restriction on survival, whereas fecundity is affected by adult dietary restriction, a pattern reminiscent of a survival/reproduction trade-off, but across a developmental boundary. The data, in combination with previous work, thus provide a picture of the intra-specific response of a suite of traits to ecological stress.

Keywords

Fecundity Nymphalidae Stress Survival Trade-offs 

Notes

Acknowledgements

We thank Craig Fee and David Stiles for help rearing and dissecting butterflies. Ilkka Hanski, Bengt Karlsson, Craig Osenberg, Ward Watt, and the reviewers commented helpfully on the manuscript.

References

  1. Angelo MJ, Slansky Jr F (1984) Body building by insects: trade-offs in resource allocation with particular reference to migratory species. Florida Entomol 67:22–41CrossRefGoogle Scholar
  2. Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Ann Rev Entomol 47:817–844PubMedCrossRefGoogle Scholar
  3. Berwaerts K, van Dyck H, Aerts P (2002) Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Funct Ecol 16:484–491CrossRefGoogle Scholar
  4. Boggs CL (1981) Nutritional and life history determinants of resource allocation in holometabolous insects. Am Nat 117:692–709CrossRefGoogle Scholar
  5. Boggs CL (1986) Reproductive strategies of female butterflies: variation in and constraints on fecundity. Ecol Entomol 11:7–15Google Scholar
  6. Boggs CL (1987) Within population variation in the demography of Speyeria mormonia (Lepidoptera: Nymphalidae). Holarctic Ecol 10:175–184Google Scholar
  7. Boggs CL (1990) A general model of the role of male-donated nutrients in female insects’ reproduction. Am Nat 136:598–617CrossRefGoogle Scholar
  8. Boggs CL (1995) Male nuptial gifts: phenotypic consequences and evolutionary implications. In: Leather SR, Hardie J (eds) Insect reproduction. CRC, New York, pp 215–242Google Scholar
  9. Boggs CL (1997) Dynamics of reproductive allocation from juvenile and adult feeding: radiotracer studies. Ecology 78:192–202CrossRefGoogle Scholar
  10. Boggs CL (2003) Environmental variation, life histories and allocation. In: Boggs CL, Watt WB, Ehrlich PR (eds) Butterflies: Ecology and Evolution Taking Flight. University of Chicago Press, Chicago, IL, pp 185–206Google Scholar
  11. Boggs CL, Dau B (2004) Resource specialization in puddling Lepidoptera. Environ Entomol 33:1020–1024CrossRefGoogle Scholar
  12. Boggs CL, Gilbert LE (1979) Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83–84PubMedCrossRefGoogle Scholar
  13. Boggs CL, Jackson LA (1991) Mud puddling by butterflies is not a simple matter. Ecol Entomol 16:123–127Google Scholar
  14. Boggs CL, Ross CL (1993) The effect of adult food limitation on the life history traits in Speyeria mormonia (Lepidoptera: Nymphalidae). Ecology 74:433–441CrossRefGoogle Scholar
  15. Carroll AL (1994) Interactions between body size and mating history influence the reproductive success of males of a tortricid moth, Zeiraphera canadensis. Can J Zool 72:2124–2132CrossRefGoogle Scholar
  16. Chippendale AK, Chu TJF, Rose MR (1996) Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution 50:753–766CrossRefGoogle Scholar
  17. Delisle J, Bouchard A (1995) Male larval nutrition in Choristoneura rosaceana (Lepidoptera: Tortricidae): an important factor in reproductive success. Oecologia 104:508–517CrossRefGoogle Scholar
  18. Delisle J, Hardy M (1997) Male larval nutrition influences the reproductive success of both sexes of the Spruce Budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Funct Ecol 11:451–463CrossRefGoogle Scholar
  19. Dudley R (2000) The biomechanics of insect flight: form, function and evolution. Princeton University Press, PrincetonGoogle Scholar
  20. Dudley R, Srygley RB (1994) Flight physiology of neotropical butterflies: allometry of airspeeds during natural free flight. J Exp Biol 191:125–139PubMedGoogle Scholar
  21. Ernsting G, Isaaks JA, Berg MP (1992) Life cycle and food availability indices in Notiophilus biguttatus (Coleoptera, Carabidae). Ecol Entomol 17:33–42Google Scholar
  22. Fischer K, Fiedler K (2001) Effects of larval starvation on adult life-history traits in the butterfly species Lycaena tityrus (Lepidoptera: Lycaenidae). Entomol Gen 25:249–254Google Scholar
  23. Fric Z, Konvicka M (2002) Generations of the polyphenic butterfly Araschnia levana differ in body design. Evol Ecol Res 4:1017–1032Google Scholar
  24. Gwynne DT (2004) Sexual differences in response to larval food stress in two nuptial feeding orthopterans—implications for sexual selection. Oikos 105:619–625CrossRefGoogle Scholar
  25. Harshman LG, Hoffmann AA, Clark AG (1999) Selection for starvation resistance in Drosophila melanogaster: physiological correlates, enzyme activities and multiple stress responses. J Evol Biol 12:370–379CrossRefGoogle Scholar
  26. Houthoofd K et al (2002) No reduction of metabolic rate in food restricted Caenorhabditis elegans. Exp Gerontol 37:1359–1369PubMedCrossRefGoogle Scholar
  27. Karlsson B, Wickman P-O (1989) The cost of prolonged life: an experiment on a nymphalid butterfly. Funct Ecol 3:399–405CrossRefGoogle Scholar
  28. Karlsson B, Leimar O, Wiklund C (1997) Unpredictable environments, nuptial gifts and the evolution of sexual size dimorphism in insects: an experiment. Proc R Soc Lond B 264:475–479CrossRefGoogle Scholar
  29. Kingsolver JG (1999) Experimental analyses of wing size, flight, and survival in the western white butterfly. Evolution 53:1479–1490CrossRefGoogle Scholar
  30. Leather SR, Beare JA, Cooke RCA, Tuke A (1998) Are differences in life history parameters of the pine beauty moth Panolis flammea (D&S) modified by host plant quality or gender? Entomol Exp Appl 87:237–243CrossRefGoogle Scholar
  31. Leimar O, Karlsson B, Wiklund C (1994) Unpredictable food and sexual size dimorphism in insects. Proc R Soc Lond B 258:121–125CrossRefGoogle Scholar
  32. Nijhout HF, Emlen DJ (1998) Competition among body parts in the development and evolution of insect morphology. Proc Natl Acad Sci USA 95:3685–3689PubMedCrossRefGoogle Scholar
  33. O’Brien DM, Fogel ML, Boggs CL (2002) Renewable and non-renewable resources: amino acid turnover and allocation to reproduction in Lepidoptera. Proc Natl Acad Sci USA 99:4413–4418PubMedCrossRefGoogle Scholar
  34. O’Brien DM, Boggs CL, Fogel ML (2004) Making eggs from nectar: connections between butterfly life history and the importance of nectar carbon in reproduction. Oikos 105:279–291CrossRefGoogle Scholar
  35. O’Brien DM, Boggs CL, Fogel ML (2005) The amino acids used in reproduction by butterflies: a comparative study of dietary sources using compound specific stable isotope analysis. Phyiological and Biochemical Zoology, in pressGoogle Scholar
  36. Rivero A, Giron D, Casas J (2001) Lifetime allocation of juvenile and adult resources to egg production in a holometabolous insect. Proc R Soc Lond B 268:1231–1237CrossRefGoogle Scholar
  37. Scriber JM, Slansky F Jr (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26:183–211CrossRefGoogle Scholar
  38. Sculley CE, Boggs CL (1996) Mating systems and sexual division of foraging effort affect puddling behavior by butterflies. Ecol Entomol 21:193–197Google Scholar
  39. Wissinger S, Steinmetz J, Alexander JS, Brown W (2004) Larval cannibalism, time constraints, and adult fitness in caddisflies that inhabit temporary wetlands. Oecologia 138:39–47PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Center for Conservation Biology, Department of Biological SciencesStanford UniversityStanfordUSA
  2. 2.Rocky Mountain Biological LaboratoryCrested ButteUSA
  3. 3.Department of Emergency MedicineUCSF FresnoFresnoUSA

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