Skip to main content
SpringerLink
Log in

Rising temperature reduces divergence in resource use strategies in coexisting parasitoid species

  • Community ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Coexistence of species sharing the same resources is often possible if species are phylogenetically divergent in resource acquisition and allocation traits, decreasing competition between them. Developmental and life-history traits related to resource use are influenced by environmental conditions such as temperature, but thermal trait responses may differ among species. An increase in ambient temperature may, therefore, affect trait divergence within a community, and potentially species coexistence. Parasitoids are interesting models to test this hypothesis, because multiple species commonly attack the same host, and employ divergent larval and adult host use strategies. In particular, development mode (arrested or continued host growth following parasitism) has been recognized as a major organiser of parasitoid life histories. Here, we used a comparative trait-based approach to determine thermal responses of development time, body mass, egg load, metabolic rate and energy use of the coexisting Drosophila parasitoids Asobara tabida, Leptopilina heterotoma, Trichopria drosophilae and Spalangia erythromera. We compared trait values between species and development modes, and calculated trait divergence in response to temperature, using functional diversity indices. Parasitoids differed in their thermal response for dry mass, metabolic rate and lipid use throughout adult life, but only teneral lipid reserves and egg load were affected by developmental mode. Species-specific trait responses to temperature were probably determined by their adaptations in resource use (e.g. lipogenesis or ectoparasitism). Overall, trait values of parasitoid species converged at the higher temperature. Our results suggest that local effects of warming could affect host resource partitioning by reducing trait diversity in communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260

    Article  PubMed  Google Scholar 

  • Askew RR, Shaw MR (1986) Parasitoid communities: their size structure and development. In: Waage J, Greathead D (eds) Insect parasitoids. Academic, London, pp 225–264

    Google Scholar 

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

    Article  Google Scholar 

  • Baffoe KO, Dalin P, Nordlander G, Stenberg JA (2012) Importance of temperature for the performance and biocontrol efficiency of the parasitoid Perilitus brevicollis (Hymenoptera: Braconidae) on Salix. Biocontrol 57:611–618

    Article  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 

  • Berg MP, Ellers J (2010) Trait plasticity in species interactions: a driving force of community dynamics. Evol Ecol 24:617–629

    Article  Google Scholar 

  • Berg MP, Kiers ET, Driessen G, Vanderheijden MW, Kooi BW, Kuenen F, Liefting M, Verhoef HA, Ellers J (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598

    Article  Google Scholar 

  • Blackburn TM (1991a) A comparative examination of life span and fecundity in parasitoid Hymenoptera. J Anim Ecol 60:151–164

    Article  Google Scholar 

  • Blackburn TM (1991b) Evidence for a ‘fast-slow’ continuum of life–history traits among parasitoid Hymenoptera. Funct Ecol 5:65–74

    Article  Google Scholar 

  • Bochdanovits Z, De Jong G (2003) Temperature dependence of fitness components in geographical populations of Drosophila melanogaster: changing the association between size and fitness. Biol J Linn Soc 80:717–725

    Article  Google Scholar 

  • Boivin G (2010) Phenotypic plasticity and fitness in egg parasitoids. Neotrop Entomol 39:457–463

    Article  PubMed  Google Scholar 

  • Canham CD, Kobe RK, Latty EF, Chazdon RL (1999) Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia 121:1–11

    Article  Google Scholar 

  • Carmona CP, Azcárate FM, de Bello F, Ollero HS, Lepš J, Peco B (2012) Taxonomical and functional diversity turnover in Mediterranean grasslands: interactions between grazing, habitat type and rainfall. J Appl Ecol 49:1084–1093

    Article  Google Scholar 

  • Carton Y, Boulétreau M, van Alphen JJM, Van Lenteren JC (1986) The Drosophila parasitic wasps. In: Ashburner M, Carson HL (eds) The genetics and biology of Drosophila (volume 3). Academic, London, pp 347–394

    Google Scholar 

  • Cavieres G, Sabat P (2008) Geographic variation in the response to thermal acclimation in rufous-collared sparrows: are physiological flexibility and environmental heterogeneity correlated? Funct Ecol 22:509–515

    Article  Google Scholar 

  • Chase JM, Leibold MA (2003) Ecological niches linking classical and contemporary approaches. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Clarke A (1993) Seasonal acclimatization and latitudinal compensation in metabolism—Do they exist? Funct Ecol 7:139–149

    Article  Google Scholar 

  • Cohen JE, JonssonT Muller CB, Godfray HCJ, Savage VM (2005) Body sizes of hosts and parasitoids in individual feeding relationships. Proc Natl Acad Sci USA 102:684–689

    Article  CAS  PubMed  Google Scholar 

  • Coleman JS, Bazzaz FA (1992) Effects of CO2 and temperature on growth and resource use of co-occurring C3 and C4 annuals. Ecology 73:1244–1259

    Article  Google Scholar 

  • Colinet H, Boivin G, Hance T (2007) Manipulation of parasitoid size using the temperature-size rule: fitness consequences. Oecologia 152:425–433

    Article  CAS  PubMed  Google Scholar 

  • Dosdall LM, Zalucki MP, Tansey JA, Fur long MJ (2012) Developmental responses of the diamondback moth parasitoid Diadegma semiclausum (Hellén) (Hymenoptera: Ichneumonidae) to temperature and host plant species. B Entomol Res 102:373–384

    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 

  • Eijs IEM, Ellers J, Van Duinen DG (1998) Feeding strategies in drosophilid parasitoids: the impact of natural food resources on energy reserves in females. Ecol Entomol 23:133–138

    Article  Google Scholar 

  • Ellers J (1996) Fat and eggs: an alternative method to measure the trade–off between survival and reproduction in insect parasitoids. Neth J Zool 46:227–235

    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, Sevenster JG, Driessen G (2000) Egg load evolution in parasitoids. Am Nat 156:650–665

    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 

  • Fleury F, Gibert P, Ris N, Allemand R (2009) Ecology and life history evolution of frugivorous Drosophila parasitoids. Adv Parasitol 70:3–44

    Article  PubMed  Google Scholar 

  • Foray V, Gibert P, Desouhant E (2011) Differential thermal performance curves in response to different habitats in the parasitoid Venturia canescens. Naturwissenschaften 98:683–691

    Article  CAS  PubMed  Google Scholar 

  • Geister TL, Lorenz MW, Hoffmann KH, Fischer K (2009) Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly. J Comp Phys B 179:87–98

    Article  Google Scholar 

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entom 52:107–126

    Article  CAS  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 (2008) Comparing and contrasting development and reproductive strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae). Evol Ecol 22:153–166

    Article  Google Scholar 

  • Harvey JA, Witjes LMA (2005) Comparing and contrasting life history and development strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae). Appl Entomol Zool 40:309–316

    Article  Google Scholar 

  • Harvey JA, Bezemer TM, Gols R, Nakamatsu Y, Tanaka T (2008) Comparing the physiological effects and function of larval feeding in closely-related endoparasitoids (Braconidae: Microgastrinae). Physiol Entomol 33:217–225

    Article  Google Scholar 

  • Harvey JA, Poelman EH, Tanaka T (2013) Intrinsic inter- and intraspecific competition in parasitoid wasps. Annu Rev Entom 58:333–351

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  • IPCC (2007) Working group I report, climate change 2007: “the physical science basis”. The fourth assessment report of the intergovernmental panel on climate change, Paris

    Google Scholar 

  • Irz P, Michonneau F, Oberdorff T, Whittier TR, Lamouroux N, Mouillot D, Argillier C (2007) Fish community comparisons along environmental gradients in lakes of France and northeast USA. Glob Ecol Biogeogr 16:350–366

    Article  Google Scholar 

  • Jervis MA, Heimpel GE, Ferns PN, Harvey JA, Kidd NAC (2001) Life-history strategies in parasitoid wasps: a comparative analysis of “ovigeny”. J Anim Ecol 70:442–458

    Article  Google Scholar 

  • Jervis MA, Ellers J, Harvey JA (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu Rev Entomol 53:361–385

    Article  CAS  PubMed  Google Scholar 

  • Jervis MA, Moe A, Heimpel GE (2012) The evolution of parasitoid fecundity: a paradigm under scrutiny. Ecol Lett 15:357–364

    Article  Google Scholar 

  • Laliberté E, Shipley B (2011) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R Package 10–11

  • Le Lann C, Roux O, Serain N, van Alphen JJM, Vernon P, van Baaren J (2011a) Thermal tolerance of sympatric hymenopteran parasitoid species: does it match their seasonal activities? Physiol Entomol 36:21–28

    Article  Google Scholar 

  • Le Lann C, Wardziak T, van Baaren J, van Alphen JJM (2011b) Plasticity in metabolic rates and life history traits affects foraging behaviour in a parasitic wasp. Funct Ecol 25:641–651

    Article  Google Scholar 

  • Le Lann C, Visser B, van Baaren J, van Alphen JJM, Ellers J (2012) Comparing resource exploitation and allocation of two closely related aphid parasitoids sharing the same host. Evol Ecol 26:79–94

    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 

  • Luo LG, Ding GH, Ji X (2010) Income breeding and temperature-induced plasticity in reproductive traits in lizards. J Exp Biol 213:2073–2078

    Article  PubMed  Google Scholar 

  • MacArthur RH, Levins R (1967) The limiting similarity convergence and divergence of coexisting species. Am Nat 101:377–385

    Article  Google Scholar 

  • Mayhew PJ, Blackburn TM (1999) Does parasitoid development mode organize life-history traits in the parasitoid Hymenoptera? J Anim Ecol 68:906–916

    Article  Google Scholar 

  • Mitchell SE, Halves J, Lampert W (2004) Coexistence of similar genotypes of Daphnia magna in intermittent populations: response to thermal stress. Oikos 106:469–478

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pavoine S, Bonsall M (2011) Measuring biodiversity to explain community assembly: a unified approach. Biol Rev 86:792–812

    Article  CAS  PubMed  Google Scholar 

  • Pelosse P, Bernstein C, Desouhant E (2007) Differential energy allocation as an adaptation to different habitats in the parasitic wasp Venturia canescens. Evol Ecol 21:669–685

    Article  Google Scholar 

  • Petchey OL, Beckerman AP, Riede JO, Warren PH (2008) Size, foraging, and food web structure. Proc Natl Acad Sci USA 105:4191–4196

    Article  CAS  PubMed  Google Scholar 

  • Price PW (1972) Parasitoids utilizing the same host: adaptive nature of differences in size and form. Ecology 53:190–195

    Article  Google Scholar 

  • Price PW (1973) Reproductive strategies in parasitoid wasps. Am Nat 107:684–693

    Article  Google Scholar 

  • Price PW (1974) Strategies for egg production. Evolution 28:76–84

    Article  Google Scholar 

  • Qu YF, Li H, Gao JF, Ji X (2011) Embryonic thermosensitivity and hatchling morphology differ between two coexisting lizards. Acta Oecol 37:375–380

    Article  Google Scholar 

  • R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3–900051–07–0 [WWW document]. Available from http://wwwR-projectorg [Accessed Nov 2010]

  • Reale D, McAdam AG, Boutin S, Berteaux D (2003) Genetic and plastic responses of a northern mammal to climate change. Proc R Soc Lond B 270:591–596

    Article  Google Scholar 

  • Romani R, Isidoro N, Bin F, Vinson SB (2002) Host recognition in the pupal parasitoid Trichopria drosophilae: a morpho-functional approach. Entomol Exp Appl 105:119–128

    Article  CAS  Google Scholar 

  • Tilman D (1982) Ressource competition and community structure. Princeton University Press, Princeton

    Google Scholar 

  • Traynor RE, Mayhew PJ (2005) A comparative study of body size and clutch size across the parasitoid Hymenoptera. Oïkos 109:305–316

    Google Scholar 

  • Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936

    Article  Google Scholar 

  • van Baaren J, Le Lann C, van Alphen JJM (2010) Consequences of climate change on aphid-based multi-trophic systems. In: Kindlmann P, Dixon AFG, Michaud JP (eds) Aphid biodiversity under environmental change: Patterns and processes. Springer, Dordrecht, pp 55–68

    Chapter  Google Scholar 

  • van Strien-van Liempt WTFH (1983) The competition between Asobara Tabida Nees Von Esenbeck, 1834 and Leptopilina Heterotoma (Thomson, 1862) in multiparasitized hosts. Neth J Zool 33:125–163

    Article  Google Scholar 

  • Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301

    Article  PubMed  Google Scholar 

  • Vinson SB (1988) Physiological studies of parasitoids reveal new approaches to the biological control of insect pests. ISI Atlas of Science 1:25–32

    Google Scholar 

  • Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252

    Article  PubMed  Google Scholar 

  • Visser B, Ellers J (2008) Lack of lipogenesis in parasitoids: a review of physiological mechanisms and evolutionary implications. J Insect Physiol 54:1315–1322

    Article  CAS  PubMed  Google Scholar 

  • Visser B, Le Lann C, den Blanken FJ, Harvey JA, van Alphen JJM, Ellers J (2010) Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle. Proc Natl Acad Sci USA 107:8677–8682

    Article  CAS  PubMed  Google Scholar 

  • Visser B, Roelofs D, Hahn DA, Teal PEA, Mariën J, Ellers J (2012) Transcriptional changes associated with lack of lipid synthesis in parasitoids. Gen Biol Evol 4:864–874

    CAS  Google Scholar 

  • Wu GM, Barrette M, Boivin G, Brodeur J, Giraldeau LA, Hance T (2011) Temperature influences the handling efficiency of an aphid parasitoid through body size-mediated effects. Environ Entomol 40:737–742

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank André T.C. Dias for helpful advice on earlier drafts of this manuscript. This research was supported by grants to C.L.L. from the Ministère de l’Enseignement Supérieur et de la Recherche and Rennes Métropole (France), by the COMPAREVOL program (Marie Curie Excellence Chair, http://comparevol.univ-rennes1.fr/) and by the ECOCLIM program founded by the Région Bretagne (France). B.V. was funded by Netherlands Organisation for Scientific Research (NWO) ALW Grant 816.01.013. The authors declare that they have no conflict of interest. The experiments comply with the current laws of the countries (The Netherlands and France) in which they were performed.

Author information

Authors and Affiliations

  1. Department of Ecological Science, VU University Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands

    Cécile Le Lann & Jacintha Ellers

  2. Institut de Recherche sur la Biologie de l’Insecte, Université de Tours, IRBI UMR CNRS, 7261, Av. Monge, 37200, Tours, France

    Bertanne Visser

  3. Unité Mixte de Recherche CNRS 6553, ECOBIO, Université de Rennes 1, 35042, Rennes Cedex, France

    Cécile Le Lann, Maëlle Mériaux & Joan van Baaren

  4. Département de Sciences Biologiques, Institut de Recherche en Biologie Végétale, Université de Montréal, 4101 Sherbrooke Est, Montreal, QC, H1X 2B2, Canada

    Joffrey Moiroux

  5. Horticultural Research and Development Centre, Agriculture and Agri-Food Canada, 430 Boulevard Gouin, St-Jean-sur-Richelieu, QC, J3B 3E6, Canada

    Joffrey Moiroux

  6. Center for Biodiversity Naturalis, P.O. Box 9517, 2300 RA, Leiden, The Netherlands

    Jacques J. M. van Alphen

  7. IBED, University of Amsterdam, P.O. Box 94248, 1090 GE, Amsterdam, The Netherlands

    Jacques J. M. van Alphen

Authors
  1. Cécile Le Lann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bertanne Visser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maëlle Mériaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joffrey Moiroux
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joan van Baaren
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jacques J. M. van Alphen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jacintha Ellers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cécile Le Lann.

Additional information

Communicated by Thomas S. Hoffmeister.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le Lann, C., Visser, B., Mériaux, M. et al. Rising temperature reduces divergence in resource use strategies in coexisting parasitoid species. Oecologia 174, 967–977 (2014). https://doi.org/10.1007/s00442-013-2810-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2810-9

Keywords

Search

Navigation