Journal of Insect Behavior

, Volume 25, Issue 2, pp 166–182 | Cite as

Aggregative Behavior is Not Explained by an Allee Effect in the Walnut Infesting Fly, Rhagoletis juglandis

Article

Abstract

Component Allee effects are considered to be a driving force in the origin and maintenance of aggregative behavior. In this study, we examine whether a pattern of active host reuse by the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), involves an Allee effect. We examined how the density of clutches deposited within a fruit, the temporal pattern in which successive clutches are deposited and the spatial distribution of clutches over a fruit’s surface influences survival to pupation and pupal size. Within the density range used in this experiment (1 to 7 clutches), increases in larval density strongly reduced pupal weight but not larval survival to pupation. The temporal staggering of clutches into a host strongly reduced offspring survival and, probably owing to competitive release, increased the pupal weight of survivors. Offspring survival and pupal weight were affected relatively little by whether two clutches were deposited within the same oviposition punctures or were evenly spaced. In contrast, in three-clutch treatments offspring survival was higher when clutches were placed within the same oviposition cavity. However, pupal weights did not significantly increase when clutches were placed together and this relatively higher survival rate was not greater than that associated with hosts that contained fewer clutches. The results of the study failed to provide evidence of an Allee effect. We put forward a scenario under which females appear to reuse larval hosts to maximize their own reproductive success, albeit at the expense of the per capita fitness of their offspring.

Key words

Allee effect marking pheromone offspring fitness parent-offspring conflict reproductive trade-offs Rhagoletis juglandis Tephritidae 

References

  1. Averill AL, Prokopy RJ (1987) Intraspecific competition in the Tephritid fruit-fly Rhagoletis pomonella. Ecology 68:878–886CrossRefGoogle Scholar
  2. Bush GL (1966) The taxonomy, cytology and evolution of the genus Rhagoletis in North America (Diptera: Tephritidae). Bull Mus Comp Zool Harv Univ 134:431–562Google Scholar
  3. Clark CW, Mangel M (1986) The evolutionary advantages of group foraging Theoretical Population. Biology 30:45–75Google Scholar
  4. Codella SG, Raffa KF (1995) Contributions of female oviposition patterns and larval behavior to group defense in conifer sawflies (Hymenoptera: Diprionidae). Oecologia 103:24–33CrossRefGoogle Scholar
  5. Corbet SA (1973) Oviposition pheromone in larval mandibular glands of Ephestia kuehniella. Nature 243:537–538PubMedCrossRefGoogle Scholar
  6. Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410PubMedCrossRefGoogle Scholar
  7. Courtney SP, Kibota TT, Singleton TA (1990) Ecology of mushroom-feeding Drosophilidae. Adv Ecol Res 20:225–275CrossRefGoogle Scholar
  8. Diaz-Fleischer F, Aluja M (2003) Influence of conspecific presence, experience, and host quality on oviposition behavior and clutch size determination in Anastrepha ludens (Diptera: Tephritidae). J Insect Behav 16:537–554CrossRefGoogle Scholar
  9. Dukas R, Prokopy RJ, Duan JJ (2001) Effects of larval competition on survival and growth in Mediterranean fruit flies. Ecol Entomol 26:587–593CrossRefGoogle Scholar
  10. Ellis AM (2008) Incorporating density dependence into the oviposition preference—offspring performance hypothesis. J Anim Ecol 77:247–256PubMedCrossRefGoogle Scholar
  11. Etienne R, Wertheim B, Hemerik L, Schneider P, Powell J (2002) The interaction between dispersal, the Allee effect and scramble competition affects population dynamics. Ecol Model 148:153–168CrossRefGoogle Scholar
  12. Fletcher LE (2009) Examining potential benefits of group living in a sawfly larva, Perga affinis. Behav Ecol 20:657–664CrossRefGoogle Scholar
  13. Gascoigne J, Berec L, Gregory S, Courchamp F (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol 51:355–372CrossRefGoogle Scholar
  14. Guedes RNC, Guedes NMP, Smith RH (2007) Larval competition within seeds: From the behaviour process to the ecological outcome in the seed beetle Callosobruchus maculatus. Austral Ecology 32:697–707CrossRefGoogle Scholar
  15. Harris MO, Anderson KG, Anderson KM, Kanno H (2006) Proximate cues for reduced oviposition by Hessian fly on wheat plants attacked by conspecific larvae. Environ Entomol 35:83–93CrossRefGoogle Scholar
  16. Hausmann SM, Miller JR (1989) Ovipositional preference and larval survival of the onion maggot (Diptera: Anthomyiidae) as influenced by previous maggot feeding. J Econ Entomol 82:426–429Google Scholar
  17. Howard DJ, Bush GL (1989) Influence of bacteria on larval survival and development in Rhagoletis (Diptera: Tephritidae). Ann Entomol Soc Am 82:633–640Google Scholar
  18. Howard DJ, Bush GL, Breznak JA (1985) The evolutionary significance of bacteria associated with Rhagoletis. Evolution 39:405–417CrossRefGoogle Scholar
  19. Huang SL, Singh M, Kojima K (1971) Study of frequency-dependent selection observed in esterase-6 of locus of Drosophila melanogaster using a conditioned media method. Genetics 68:97–104PubMedGoogle Scholar
  20. Klok CJ, Chown SL (1999) Assessing the benefits of aggregation: thermal biology and water relations of anomalous Emperor Moth caterpillars. Funct Ecol 13:417–427CrossRefGoogle Scholar
  21. Kramer AM, Dennis B, Liebhold AM, Drake JM (2009) The evidence for Allee effects. Popul Ecol 51:341–354CrossRefGoogle Scholar
  22. Lalonde RG, Mangel M (1994) Seasonal effects on superparasitism by Rhagoletis completa. J Anim Ecol 63:583–588CrossRefGoogle Scholar
  23. Lam K, Babor D, Duthie B, Babor EM, Moore M, Gries G (2007) Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies. Anim Behav 74:81–92CrossRefGoogle Scholar
  24. Lockwood JA, Story RN (1985) Photic, thermic, and sibling influences on the hatching rhythm of the southern green stink bug, Nezara viridula (L). Environ Entomol 14:562–567Google Scholar
  25. Magro A, Tene JN, Bastin N, Dixon AFG, Hemptinne JL (2007) Assessment of patch quality by ladybirds: relative response to conspecific and heterospecific larval tracks a consequence of habitat similarity? Chemoecology 17:37–45CrossRefGoogle Scholar
  26. Mappes J, Mäkelä I (1993) Egg and larval load assessment and its influence on oviposition behavior of the leaf beetle Galerucella nymphaeae. Oecologia 93:38–41Google Scholar
  27. Nufio CR, Papaj DR (2001) Host marking behavior in phytophagous insects and parasitoids. Entomol Exp Appl 99:273–293CrossRefGoogle Scholar
  28. Nufio CR, Papaj DR (2004a) Superparasitism of larval hosts by the walnut fly, Rhagoletis juglandis, and its implications for female and offspring performance. Oecologia 141:460–467PubMedCrossRefGoogle Scholar
  29. Nufio CR, Papaj DR (2004b) Host-marking behaviour as a quantitative signal of competition in the walnut fly Rhagoletis juglandis. Ecol Entomol 29:336–344CrossRefGoogle Scholar
  30. Nufio CR, Papaj DR, Alonso-Pimentel H (2000) Host utilization by the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Environ Entomol 29:994–1001CrossRefGoogle Scholar
  31. Nylin S, Janz N, Wedell N (1996) Oviposition plant preference and offspring performance in the comma butterfly: Correlations and conflicts. Entomol Exp Appl 80:141–144CrossRefGoogle Scholar
  32. Paine TD, Raffa KF, Harrington TC (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu Rev Entomol 42:179–206PubMedCrossRefGoogle Scholar
  33. Papaj DR (ed) (1993) Use and avoidance of occupied hosts as a dynamic process in tephritid fruit flies. CRC, Boca Raton, pp 25–46Google Scholar
  34. Papaj DR, Alonso-Pimentel H (1997) Why walnut flies superparasitize: Time savings as a possible explanation. Oecologia 109:166–174CrossRefGoogle Scholar
  35. Parrish JK, Edelstein-Keshet L (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284:99–101PubMedCrossRefGoogle Scholar
  36. Prokopy RJ, Duan JJ (1998) Socially facilitated egglaying behavior in Mediterranean fruit flies. Behav Ecol Sociobiol 42:117–122CrossRefGoogle Scholar
  37. Prokopy RJ, Roitberg BD (2001) Joining and avoidance behavior in nonsocial insects. Annu Rev Entomol 46:631–665PubMedCrossRefGoogle Scholar
  38. Rausher MD (1980) Host abundance, juvenile survival, and oviposition preference in Battus philenor. Evolution 34:342–355CrossRefGoogle Scholar
  39. Reader T, Hochuli DF (2003) Understanding gregariousness in a larval Lepidopteran: the roles of host plant, predation, and microclimate. Ecol Entomol 28:729–737CrossRefGoogle Scholar
  40. Sang JH (1956) The quantitative nutritional requirements of Drosophila melanogaster. J Exp Biol 33:45–72Google Scholar
  41. SAS (2000) JMP, Version 4. Statistics and Graphics Guide. SAS InstituteGoogle Scholar
  42. Scheirs J, De Bruyn L (2002) Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96:187–191CrossRefGoogle Scholar
  43. Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87:185–190CrossRefGoogle Scholar
  44. Takasu K, Hirose Y (1988) Host discrimination in the parasitoid ooencyrtus nezarae: the role of egg stalk as an external marker. Entomol Exp Appl 47:45–48CrossRefGoogle Scholar
  45. Telang A, Hammond SS, Opp SB (1996) Effects of copulation frequency on egg-laying and egg hatch in the walnut husk fly, Rhagoletis completa Cresson. Pan-Pacific Entomologist 72:235–237Google Scholar
  46. van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu Rev Entomol 35:59–79PubMedCrossRefGoogle Scholar
  47. Wertheim B, Marchais J, Vet LEM, Dicke M (2002) Allee effect in larval resource exploitation in Drosophila: an interaction among density of adults, larvae, and micro-organisms. Ecol Entomol 27:608–617CrossRefGoogle Scholar
  48. Wertheim B, van Baalen EJA, Dicke M, Vet LEM (2005) Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annu Rev Entomol 50:321–346PubMedCrossRefGoogle Scholar
  49. Wise MJ, Kieffer DL, Abrahamson WG (2006) Costs and benefits of gregarious feeding in the meadow spittlebug, Philaenus spumarius. Ecol Entomol 31:548–555CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary Biology and University of Colorado Natural History MuseumUniversity of ColoradoBoulderUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

Personalised recommendations