Skip to main content
Log in

Manipulation of parasitoid size using the temperature-size rule: fitness consequences

  • Ecophysiology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The phenotypic effects of rearing temperature on several fitness components of the koinobiont parasitoid, Aphidius colemani, were examined. Temperatures experienced during development induced a plastic linear response in the dry and fat masses of the immature stage and a non-linear response in the growth rate as well as in the size of adults. We investigated if the phenotypic morphometrical plasticity exhibited by parasitoids reared at different temperatures can induce variations in fitness-related traits in females. We did not find any difference in immature (pupal) mortality in accordance to rearing temperature. However, when examining adult longevity, we found an inverse linear relation with developmental temperature, confirming the usual rule that larger and fatter wasps live longer than smaller ones. The pattern of female fecundity was non-linear; wasps that developed at high and low temperatures were less productive. We suggest that when development is short, the accumulated reserves are not adequate to support both fecundity and survival. By manipulating adult size through changes in the rearing temperature, we showed that the usual shape of the size/fitness function is not always linear as expected. Developmental temperature induced a plasticity in energy reserves which affected the functional constraints between survival and reproduction.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Angilletta MJ, Dunham AE (2003) The temperature-size rule in ectotherms: simple evolutionary explanations may not be general. Am Nat 162:332–342

    Article  PubMed  Google Scholar 

  • Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    Article  Google Scholar 

  • Atkinson D (1994) Temperature and organism size – a biological law for ectotherms? Adv Ecol Res 25:1–58

    Google Scholar 

  • Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Tree 12:235–239

    Google Scholar 

  • Bazzocchi GG, Lanzoni A, Burgio G, Fiacconi MR (2003) Effects of temperature and host on the pre-imaginal development of the parasitoid Diglyphus isaea (Hymenoptera: Eulophidae). Biol Control 26:74–82

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Birkemoe T, Leinaas HP (2000) Effects of temperature on the development of an arctic Collembola (Hypogastrura tullbergi). Funct Ecol 14:693–700

    Article  Google Scholar 

  • Blanckenhorn WU (1997) Effects of temperature on growth, development and diapause in the yellow dung fly – against all the rules? Oecologia 111:318–324

    Article  Google Scholar 

  • Blanckenhorn WU (2000) Temperature effects on egg size and their fitness consequences in the yellow dung fly Scathophaga stercoraria. Evol Ecol 14:627–643

    Article  Google Scholar 

  • Bochdanovits Z, de Jong G (2003) Temperature dependent larval resource allocation shaping adult body size in Drosophila melanogaster. J Evol Biol 16:1159–1167

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Cambier V, Hance Th De Hoffmann E (2001) Effects of 1,4-benzoxazin-3-one derivatives from maize on survival and fecundity of Metopolophium dirhodum (Walker) on artificial diet. J Chem Ecol 27:359–370

    Article  PubMed  CAS  Google Scholar 

  • Casas J, Pincebourde S, Mandon N, Vannier F, Poujol R, Giron D (2005) Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology 86:545–554

    Google Scholar 

  • Cavicchi S, Guerra D, Natali V, Pezzoli C, Giorgi G (1989) Temperature-related divergence in experimental populations of Drosophila melanogaster. II. Correlations between fitness and body dimensions. J Evol Biol 2:235–251

    Article  Google Scholar 

  • Cloutier C, McNeil JN, Regnière J (1981) Fecundity, longevity and sex ratio of Aphidius nigripes (Hymenoptera: Aphidiidae) parasiting different stages of its host, Macrosiphum euphorbiae (Homoptera: Aphididae). Can Entomol 113:193–198

    Google Scholar 

  • Colinet H, Salin C, Boivin G, Hance Th (2005) Host age and fitness-related traits in a koinobiont aphid parasitoid. Ecol Entomol 30:473–479

    Article  Google Scholar 

  • Colinet H, Hance T, Vernon P (2006) Water relations, fat reserves, survival and longevity of a cold-exposed parasitic wasp Aphidius colemani (Hymenoptera: Aphidiidae). Environ Entomol 35:228–236

    Article  Google Scholar 

  • David JR, Moreteau B, Gautier JP, Pétavy G, Stockel A, Imasheva AG (1994) Reaction norms of size characters in relation to growth temperature in Drosophila melanogaster: an isofemale lines analysis. Genet Sel Evol 26:229–251

    Google Scholar 

  • De Vis RMJ, Fuentes LE, van Lenteren JC (2002) Life history of Amitus fuscipennis (Hym., Platygastridae) as parasitoid of the greenhouse whitefly Trialeurodes vaporariorum (Hom., Aleyrodidae) on tomato as function of temperature. J Appl Entomol 126:24–33

    Article  Google Scholar 

  • Deng YX, Tsai JH (1998) Development of Lysiphlebia japonica (Hymenoptera: Aphidiidae), a parasitoid of Toxoptera citricida (Homoptera: Aphididae) at five temperatures. Fla Entomol 81:415–423

    Article  Google Scholar 

  • Eijs IEM, van Alphen JJM (1999) Life history correlations: why are hymenopteran parasitoids an exception? Ecol Lett 2:27–35

    Article  Google Scholar 

  • Ellers J, van Alphen JJM (1997) Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction. J Evol Biol 10:771–785

    Article  Google Scholar 

  • Ellers J, van Alphen JJM, Sevenster JG (1998) A field study of size–fitness relationships in the parasitoid Asobara tabida. J Anim Ecol 67:318–324

    Article  Google Scholar 

  • Ellers J, Driessen G, Sevenster JG (2000) The shape of the trade-off function between reproduction and survival in the parasitoid Asobara tabida. Neth J Zool 50:29–36

    Article  Google Scholar 

  • Ellers J, Bax M, van Alphen JJM (2001) Seasonal changes in female size and its relation to reproduction in the parasitoid Asobara tabida. Oikos 92:309–314

    Article  Google Scholar 

  • Elliott NC, Burd JD, Kindler SD, Lee JH (1995) Temperature effects on development of three cereal aphid parasitoids (Hymenoptera: Aphididae). Great Lakes Entomol 28:199–204

    Google Scholar 

  • Giron D, Casas J (2003) Lipogenesis in an adult parasitic wasp. J Insect Physiol 49:141–147

    Article  PubMed  CAS  Google Scholar 

  • Godfray HCJ (1994) Parasitoids, behavioral and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  • Harvey JA (2005) Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomol Exp Appl 117:1–13

    Article  Google Scholar 

  • Harvey JA, Strand MR (2002) The developmental strategies of endoparasitoid wasps vary with host feeding ecology. Ecology 83:2439–2451

    Article  Google Scholar 

  • Harvey JA, Kadash K, Strand MR (2000) Differences in larval feeding behavior correlate with altered development strategies in two parasitic wasps: implications for the size-fitness hypothesis. Oikos 88:621–629

    Article  Google Scholar 

  • Harvey JA, Bezemer TM, Elzinga JA, Strand MR (2004) Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size. Ecol Entomol 29:35–43

    Article  Google Scholar 

  • Hofsvang T, Hagvar EB (1975) Duration of development and longevity in Aphidius ervi and Aphidius platensis (Hymenoptera: Aphidiidae), two parasites of Myzus persicae (Homoptera: Aphididae). Entomophaga 20:11–22

    Article  Google Scholar 

  • Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity in ectotherms. Trends Ecol Evol 4:131–135

    Article  Google Scholar 

  • Ichiki R, Takasu K, Shima H (2003) Effects of temperature on immature development of the parasitic fly Bessa parallela (Meigen) (Diptera: Tachinidae). Appl Entomol Zool 38:435–439

    Article  Google Scholar 

  • Jann P, Ward PI (1999) Maternal effects and their consequences for offspring fitness in the Yellow Dung Fly. Funct Ecol 23:51–58

    Article  Google Scholar 

  • Jervis MA, Ferns PN, Heimpel GE (2003) Body size and the timing of egg production in parasitoid wasps: a comparative analysis. Funct Ecol 17:375–383

    Article  Google Scholar 

  • Karan D, Morin JP, Moreteau B, David JR (1998) Body size and developmental temperature in Drosophila melanogaster: analysis of body weight reaction norm. J Therm Biol 23:301–309

    Article  Google Scholar 

  • Kouame KL, Mackauer M (1991) Influence of aphid size, age and behaviour on host choice by the parasitoid wasp Ephedrus californicus – a test of host-size models. Oecologia 88:197–203

    Article  Google Scholar 

  • Lamb RJ, Gerber GH (1985) Effects of temperature on the development, growth, and survival of larvae and pupae of a north-temperate chrysomelid beetle. Oecologia 67:8–18

    Article  Google Scholar 

  • Leather SR (1988) Size, reproductive potential and fecundity in insects: things aren’t as simple as they seem. Oikos 51:386–389

    Article  Google Scholar 

  • Li B, Mills N (2004) The influence of temperature on size as an indicator of host quality for the development of a solitary koinobiont parasitoid. Entomol Exp Appl 110:249–256

    Article  Google Scholar 

  • Nealis VG, Jones RE, Wellington WG (1984) Temperature and development in host–parasite relationships. Oecologia 61:224–229

    Article  Google Scholar 

  • Nijhout HF (1994) Insect hormones. Princeton University Press, Princeton

    Google Scholar 

  • Nunney L, Cheung W (1997) The effect of temperature on body size and fecundity in female Drosophila melangonaster – evidence for adaptive plasticity. Evolution 51:1529–1535

    Article  Google Scholar 

  • Nylin S, Gotthard K (1998) Plasticity in life-history traits. Annu Rev Entomol 43:63–83

    Article  PubMed  CAS  Google Scholar 

  • Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy fitness. Annu Rev Entomol 51:163–185

    Article  PubMed  CAS  Google Scholar 

  • Ohgushi T (1996) Consequences of adult size for survival and reproductive performance in a herbivorous ladybird beetle. Ecol Entomol 21:47–55

    Google Scholar 

  • Olson DM, Fadamiro H, Lundgren JOG, Heimpel GE (2000) Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp. Physiol Entomol 25:17–26

    Article  CAS  Google Scholar 

  • Pandey S, Singh R (1999) Host size induced variation in sex ratio of an aphid parasitoid Lysiphlebia mirizai. Entomol Exp Appl 90:61–67

    Article  Google Scholar 

  • Partridge L, Barrie B, Fowler K, French V (1994) Thermal evolution of pre-adult life history traits in Drosophila melanogaster. J Evol Biol 7:645–663

    Article  Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Tree 20:481–486

    PubMed  Google Scholar 

  • Powell JR (1974) Temperature related divergence in Drosophila body size. J Hered 65:257–258

    PubMed  CAS  Google Scholar 

  • Ris N (2003) Hétérogénéité spatiale, plasticité phénotypique et trade-off environnementaux: Rôle de l’espèce hôte et de la température dans la différenciation génétique des populations du parasitoïde Leptopilina heterotoma (Hymenoptera). PhD thesis, Université Claude Bernard, Lyon

  • Ris N, Allemand R, Fouillet P, Fleury F (2004) The joint effect of temperature and host species induce complex genotype-by-environment interactions in the larval parasitoid of Drosophila, Leptopilina heterotoma (Hymenoptera: Figitidae). Oikos 106:451–456

    Article  Google Scholar 

  • Rivero A, Casas J (1999) Incorporating physiology into parasitoid behavioral ecology: the allocation of nutritional resources. Res Popul Ecol 41:39–45

    Article  Google Scholar 

  • Rivero A, West SA (2002) The physiological costs of being small in a parasitic wasp. Evol Ecol Res 4:407–420

    Google Scholar 

  • Röhne O (2002) Effect of temperature and host stage on preference of Aphelinus varipes Förster (Hym., Aphelinidae) parasiting the cotton aphid, Aphis gossypii Glover (Hom., Aphididae). J Appl Entomol 126:572–576

    Article  Google Scholar 

  • Roitberg BD, Boivin G, Vet LEM (2001) Fitness, parasitoids, and biological control: an opinion. Can Entomol 133:429–438

    Article  Google Scholar 

  • Sequeira R, Mackauer M (1992) Quantitative genetics of body size and development time in the parasitoid wasp Aphidius ervi (Hymenoptera, Aphidiidae). Can J Zool 70:1102–1108

    Article  Google Scholar 

  • Sequeira R, Mackauer M (1993) Seasonal variation in body size and offspring sex ratio in field populations of the parasitoid wasp, Aphidius ervi (Hymenoptera: Aphidiidae). Oikos 68:340–346

    Article  Google Scholar 

  • Sequeira R, Mackauer M (1994) Variation in selected life-history parameters of the parasitoid wasp, Aphidius ervi: influence of host developmental stage. Entomol Exp Appl 71:15–22

    Article  Google Scholar 

  • Sibly RM, Atkinson D (1994) How rearing temperature affects optimal adult size in ectotherms. Funct Ecol 8:486–493

    Article  Google Scholar 

  • Sisodia S, Singh BN (2002) Effect of temperature on longevity and productivity in Drosophila ananassae: evidence for adaptive plasticity and trade-off between longevity and productivity. Genetica 114:95–102

    Article  PubMed  Google Scholar 

  • Starý P (1975) Aphidius colemani Viereck: its taxonomy, distribution and host range (Hymenopetra: Aphidiidae). Acta Entomol Bohemoslov 72:156–173

    Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Strohm E (2000) Factors affecting body size and fat content in a digger wasp. Oecologia 123:184–191

    Article  Google Scholar 

  • Terblanche JS, Klok CJ, Chown SL (2004) Metabolic rate variation in Glossina pallidipes (Diptera: Glossinidae): gender, ageing and repeatability. J Insect Physiol 50:419–428

    Article  PubMed  CAS  Google Scholar 

  • Van Handel E (1993) Fuel metabolism of the mosquito (Culex quinquefasciatus) embryo. J Insect Physiol 39:831–833

    Article  Google Scholar 

  • Van Steenis MJ (1993) Intrinsic rate of increase of Aphidius colemani Vier. (Hym., Braconidae) a parasitoid of Aphis gossypii Glov. (Hom., Aphididae) at different temperatures. J Appl Entomol 116:192–198

    Article  Google Scholar 

  • Visser ME (1994) The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). J Anim Ecol 63:963–978

    Article  Google Scholar 

  • West SA, Flanagan KE, Godfray HCJ (1996) The relationship between parasitoid size and fitness in the field: a study of Achrysocharoides zwoelferi (Hymenoptera, Eulophidae). J Anim Ecol 65:631–639

    Article  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1999) The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284:167–169

    Article  Google Scholar 

  • Williams I (1999) Slow-growth, high mortality a general hypothesis, or is it? Ecol Entomol 24:490–495

    Article  Google Scholar 

  • Zhao Z, Zera AJ (2002) Differential lipid biosynthesis underlies a tradeoff between reproduction and flight capability in a wing-polymorphic cricket. Proc Natl Acad Sci USA 99:16829–16834

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We sincerely thank J. Ellers, D. Giron and N. Ris for very constructive comments on the manuscript. We are also grateful to P. Baret and C. Salin for useful helps. This study was supported by “Ministère de la Région wallonne – DGTRE Division de la Recherche et de la Coopération scientifique.” FIRST EUROPE Objectif 3. This paper is BRC109 of the Biodiversity Research Centre. 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 H. Colinet.

Additional information

Communicated by Thomas Hoffmeister.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Colinet, H., Boivin, G. & Hance, T. Manipulation of parasitoid size using the temperature-size rule: fitness consequences. Oecologia 152, 425–433 (2007). https://doi.org/10.1007/s00442-007-0674-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-007-0674-6

Keywords

Navigation