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Superparasitism of larval hosts by the walnut fly, Rhagoletis juglandis, and its implications for female and offspring performance - Oecologia

  • ️Papaj, Daniel R.
  • ️Thu Aug 05 2004

Abstract

The oviposition-preference–offspring-performance hypothesis predicts that female insects should prefer to deposit clutches on or in hosts that maximize offspring performance. An important assumption behind this prediction is that female fitness is tightly correlated with the fitness of any one offspring. In this study, we evaluate offspring performance in the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), in relation to a previously described oviposition preference for previously exploited host fruit. In particular, we examined how superparasitism of walnut hosts influences offspring survival and weight at pupation under field conditions. We found that superparasitism was common and that increases in larval densities within fruit were associated with reduced larval survival and weight at pupation. In a laboratory experiment, female size was correlated with lifetime fecundity. In this system, oviposition preference is therefore negatively, not positively, correlated with offspring performance. We argue that patterns of female preference in this system reflect direct benefits to females that are traded off against costs in terms of offspring fitness. Because female fitness is a product not only of offspring quality but also of the total number of offspring produced, female walnut flies may be optimizing their fitness by producing many less fecund offspring. Studies examining the preference-performance hypothesis should consider the reproductive conflicts between parents and offspring as potential factors that influence the congruence between parental preference and offspring performance.

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References

  • van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu Rev Entomol 35:59–79

    Article  PubMed  Google Scholar 

  • van Alphen JJM, Visser ME, Nell HW (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: searching in groups vs. sequential patch visits. Funct Ecol 6:528–535

    Google Scholar 

  • Averill AL, Prokopy RJ (1987) Intraspecific competition in the tephritid fruit fly Rhagoletis pomonella. Ecology 68:878–886

    Google Scholar 

  • Ballabeni P, Wlodarczyk M, Rahier M (2001) Does enemy-free space for eggs contribute to a leaf beetle’s oviposition preference for a nutritionally inferior host plant? Funct Ecol 15:318–324

    Article  Google Scholar 

  • Bernays EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annu Rev Entomol 46:703–727

    Article  CAS  PubMed  Google Scholar 

  • Bonduriansky R, Brooks RJ (1999) Reproductive allocation and reproductive ecology of seven species of Diptera. Ecol Entomol 24b:389–395

    Article  Google Scholar 

  • Burk T, Webb JC (1983) Effect of male size on calling propensity, song parameters, and mating success in Caribbean fruit flies, Anestrepha suspensa (Loew) (Diptera, Tiphritidae). Ann Entomol Soc Am 76:678–682

    Google Scholar 

  • Bush GL (1966) The taxonomy, cytology and evolution of the genus Rhagoletis in North America (Diptera: Tephritidae). Bull Mus Comp Zool Harv Univ 134:431–562

    Google Scholar 

  • Charnov EL, Skinner SW (1985) Complementary approaches to the understanding of parasitoid oviposition decisions. Environ Entomol 14:383–391

    Google Scholar 

  • Copp NH, Davenport D (1978) Agraulis and passiflora. I. control of specificity. Biol Bull 155:98–112

    Google Scholar 

  • Courtney SP, Kibota TT (1990) Mother doesn’t know best: selection of host by ovipositing insects. In: Bernays EA (ed) Insect-plant interactions. CRC, Boca Raton, Fla., pp 161–188

    Google Scholar 

  • Craig TP, Itami JK, Price PW (1989) A strong relationship between oviposition preference and larval performance in a shoot-galling sawfly. Ecology 70:1691–1699

    Google Scholar 

  • Credland PF, Dick KM, Wright AW (1986) Relationship between larval density, adult size and egg production in the cowpea seed beetle, Callosobruchus maculatus. Ecol Entomol 11:41–50

    Google Scholar 

  • Denno RF, Larsson S, Olmstead KL (1990) Role of enemy-free space and plant quality in host–plant selection by willow beetles. Ecology 71:124–137

    Google Scholar 

  • Einum S, Fleming IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565–567

    Article  CAS  PubMed  Google Scholar 

  • Etges WJ, Heed WB (1987) Sensitivity to larval density in populations of Drosophila mojavensis: influences of host plant variation on components of fitness. Oecologia 71:375–381

    Google Scholar 

  • Forbes LS (1991) Optimal size and number of offspring in a variable environment. J Theor Biol 150:299–304

    Google Scholar 

  • Fox CW (1993) A quantitative genetic analysis of oviposition preference and larval performance on two hosts in the bruchid beetle, Callosobruchus maculatus. Evolution 47:166–175

    Google Scholar 

  • Godfray HCJ (1987) The evolution of clutch size in parasitic wasps. Am Nat 129:221–233

    Article  Google Scholar 

  • Howard DJ, Bush GL (1989) Influence of bacteria on larval survival and development in Rhagoletis (Diptera: Tephritidae). Ann Entomol Soc Am 82:633–640

    Google Scholar 

  • Howard DJ, Bush GL, Breznak JA (1985) The evolutionary significance of bacteria associated with Rhagoletis. Evolution 39:405–417

    Google Scholar 

  • Jaenike J (1978) Optimal oviposition behavior in phytophagous insects. Theor Popul Biol 14:350–356

    CAS  PubMed  Google Scholar 

  • Karban R, Courtney S (1987) Intraspecific host plant choice: lack of consequences for Streptanthus tortuosus (Cruciferae) and Euchloe hyantis (Lepidoptera: Pieridae). Oikos 48:243–248

    Google Scholar 

  • Lalonde RG, Mangel M (1994) Seasonal effects on superparasitism by Rhagoletis completa. J Anim Ecol 63:583–588

    Google Scholar 

  • Landolt PJ, Averill AL (1999) Fruit Flies. In: Hardie J, Minks AK (eds) Pheromones of non-lepidopteran insects associated with agricultural plants. CABI, New York, pp 3–26

    Google Scholar 

  • Larsson S, Ekbom B (1995) Oviposition mistakes in herbivorous insects: confusion or a step towards a new host giant. Oikos 72:155–160

    Google Scholar 

  • Leather SR (1985) Oviposition preferences in relation to larval growth rates and survival in the pine beauty moth, Panolis flammea. Ecol Entomol 10:213–217

    Google Scholar 

  • Lloyd DG (1987) Selection of offspring size at independence and other size-versus-number strategies. Am Nat 129:800–817

    Article  Google Scholar 

  • Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428

    Google Scholar 

  • Messina FJ (1982) Food plant choices of two goldenrod beetles: relation to plant quality. Oecologia 55:342–354

    Google Scholar 

  • Mills NJ, Kuhlmann U (2000) The relationship between egg load and fecundity among Trichogramma parasitoids. Ecol Entomol 25:315–324

    Article  Google Scholar 

  • Nufio CR, Papaj DR (2004) Host marking behavior as a quantitative signal of infestation levels in host use by the walnut fly, Rhagoletis juglandis. Ecol Entomol 29:336–344

    Article  Google Scholar 

  • Nufio CR, Papaj DR, Alonso-Pimentel H (2000) Host utilization by the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Environ Entomol 29:994–1001

    Google Scholar 

  • Nylin S, Janz N (1996) Host plant preferences in the comma butterfly (Polygonia calbum): do parents and offspring agree? Ecoscience 3:285–289

    Google Scholar 

  • Nylin S, Janz N, Wedell N (1996) Oviposition plant preference and offspring performance in the comma butterfly: correlations and conflicts. Entomol Exp Appl 80:141–144

    Google Scholar 

  • Papaj DR (1993) Use and avoidance of occupied hosts as a dynamic process in tephritid fruit flies. In: Bernays EA (ed) Insect-Plant Interactions. CRC, Boca Raton, Fla., pp 25–46

    Google Scholar 

  • Papaj DR (1994) Oviposition site guarding by male walnut flies and its possible consequences for mating success. Behav Ecol Sociobiol 34:187–195

    Google Scholar 

  • Papaj DR, Alonso-Pimentel H (1997) Why walnut flies superparasitize: time savings as a possible explanation. Oecologia 109:166–174

    Article  Google Scholar 

  • Price PW, Ohgushi T (1995) Preference and performance linkage in a Phyllocolpa sawfly on the willow, Salix miyabeana, on hokkaido. Res Popul Ecol 37:23–28

    Google Scholar 

  • Prokopy RJ (1981) Oviposition-deterring pheromone system of apple maggot flies. In: Mitchell EK (ed) Management of insect pests with semiochemicals. Plenum, New York, pp 477–494

    Google Scholar 

  • Rausher MD (1980) Host abundance, juvenile survival, and oviposition preference in Battus philenor. Evolution 34:342–355

    Google Scholar 

  • Rossi AM, Strong DR (1991) Effects of host-plant nitrogen on the preference and performance of laboratory populations of Carneocephala floridana (Homoptera: Cicadellidae). Environ Entomol 20:1349–1355

    Google Scholar 

  • SAS (2000) JMP, Version 4. Statistics and Graphics Guide. SAS Institute, Cary, N.C.

  • Scheirs J, De Bruyn L (2002) Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96:187–191

    Article  Google Scholar 

  • Scheirs J, De Bruyn L, Verhagen R (2000) Optimization of adult performance determines host choice in a grass miner. Proc R Soc Lond B Biol Sci 267:2065–2069

    Article  CAS  PubMed  Google Scholar 

  • Smith RH, Lessells CM (1985) Oviposition, ovicide, and larval competition in granivorous insects. In: Sibly RM, Smith RH (eds) Behavioral ecology: ecological consequences of adaptive behaviour. Blackwell, Oxford, pp 423–448

    Google Scholar 

  • Speirs DC, Sherratt TN, Hubbard SF (1991) Parasitoid diets—does superparasitism pay? Trends Ecol Evol 6:22–25

    Article  Google Scholar 

  • Taylor PW, Yuval B (1999) Postcopulatory sexual selection in Mediterranean fruit flies: advantages for large and protein fed males. Anim Behav 58:247–254

    Article  PubMed  Google Scholar 

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Google Scholar 

  • Valladares G, Lawton JH (1991) Host-plant selection in the holly leaf-miner: does mother know best? J Anim Ecol 60:227–240

    Google Scholar 

  • Weisser WW, Houston AI, Volkl W (1994) Foraging strategies in solitary parasitoids: the trade-off between female and offspring mortality risks. Evol Ecol 8:587–597

    Google Scholar 

  • Wickman PO, Karlsson B (1989) Abdomen size, body size and reproductive effort of insects. Oikos 56:209–214

    Google Scholar 

  • Wiklund C (1981) Generalist vs. specialist oviposition behavior in Papilio machaon (Lepidoptera) and functional-aspects on the hierarchy of oviposition preferences. Oikos 36:163–170

    Google Scholar 

  • Williams KS (1983) The coevolution of Euphydryas chalcedona butterflies and their larval host plants. III. Oviposition behavior and host plant quality. Oecologia 56:336–340

    Google Scholar 

Download references

Acknowledgements

We thank Henar Alonso-Pimentel, Judie Bronstein, Reginald Chapman, Laurie Henneman, Dena Smith and the Plant-Animal Interactions reading group at the University of Colorado for comments and discussion. Sheridan Stone of the Fort Huachuca Wildlife Management Office of the United States of America Army provided permission and logistical support for fieldwork in Garden Canyon. A Pre-Graduate National Science Fellowship, NRICGP grant no. 93-37302-9126 to D. R. P., and Sigma Xi grant supported this research.

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Authors and Affiliations

  1. Department of Entomology, University of Arizona, Tucson, AZ, 85721, USA

    César R. Nufio

  2. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA

    Daniel R. Papaj

  3. Center for Insect Science, University of Arizona, Tucson, AZ, 85721, USA

    Daniel R. Papaj

  4. The Interdisciplinary Degree Program in Insect Science, University of Arizona, Tucson, AZ, 85721, USA

    César R. Nufio

  5. CU Museum of Natural History, University of Colorado, UCB 265, Boulder, CO, 80309, USA

    César R. Nufio

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  1. César R. Nufio

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Nufio, C.R., Papaj, D.R. Superparasitism of larval hosts by the walnut fly, Rhagoletis juglandis, and its implications for female and offspring performance. Oecologia 141, 460–467 (2004). https://doi.org/10.1007/s00442-004-1669-1

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  • Received: 24 March 2004

  • Accepted: 30 June 2004

  • Published: 05 August 2004

  • Issue Date: November 2004

  • DOI: https://doi.org/10.1007/s00442-004-1669-1

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