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Oecologia

, Volume 179, Issue 3, pp 777–784 | Cite as

Host selection by an insect herbivore with spatially variable density dependence

  • William C. WetzelEmail author
  • Donald R. Strong
Plant-microbe-animal interactions - Original research

Abstract

Many species of phytophagous insects do not oviposit preferentially on plants that yield high offspring performance. One proposed explanation is that negatively density-dependent offspring performance would select for females that disperse eggs among plants to minimize competition. Recent work showing larval density dependence often varies substantially among plants suggests that ovipositing females should not only respond to the density of competitors but also to traits predictive of the strength of density dependence mediated by plants. In this study, we used field and greenhouse experiments to examine oviposition behavior in an insect herbivore that experiences density-dependent larval performance and variability in the strength of that density dependence among host-plant individuals. We found females moved readily among plants in the field and had strong preferences for plants that mediate weak offspring density dependence. Females, however, did not avoid plants with high densities of competitors, despite the fact that offspring performance declines steeply with density on most plants in natural populations. This means females minimize the effects of density dependence on their offspring by choosing plants that mediate only weak larval density dependence, not by choosing plants with low densities of competitors. Our results suggest that explaining the lack of positive preference-performance correlations in many systems may not be as simple as invoking density dependence. Resource selection behavior may depend not just on the presence or absence of density-dependent offspring performance but also on variation in the strength of offspring density dependence among sites within populations.

Keywords

Host-plant preference Offspring performance Oviposition behavior Tephritidae Plant–insect interaction 

Notes

Acknowledgments

We thank R. Karban, J. Rosenheim, P. Grof-Tisza, M. Meek, I. Pearse, and the University of California (UC) Davis Insect Ecology Joint Lab Group for discussion and criticism. S. Krasnobrod, M. Cruz, R. Cox, A. Jordan, C. Kaplinsky, W. Zhang, and M. Meek provided field and lab assistance. We are grateful to D. Dawson of the UC VESR where this work was conducted. The UC Davis Center for Population Biology, the UC Natural Reserve Mathias Program, and the UC VESR provided funding. W. C. W. was supported by NSF DEB 081430, the REACH IGERT at UC Davis.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Agrawal AA (2004) Plant defense and density dependence in the population growth of herbivores. Am Nat 164:113–120. doi: 10.1086/420980 CrossRefPubMedGoogle Scholar
  2. Alvarez-Cordero E, McKell CM (1979) Stem cutting propagation of big sagebrush (Artemisia tridentata Nutt.). J Range Manage 32:141–143. doi: 10.2307/3897559 CrossRefGoogle Scholar
  3. Auerbach M, Simberloff D (1989) Oviposition site preference and larval mortality in a leaf-mining moth. Ecol Entomol 14:131–140CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4Google Scholar
  5. Blaustein L, Kotler BP (1993) Oviposition habitat selection by the mosquito, Culiseta longiareolata: effects of conspecifics, food and green toad tadpoles. Ecol Entomol 18:104–108CrossRefGoogle Scholar
  6. Bolker BM (2008) Ecological models and data in R. Princeton University Press, PrincetonGoogle Scholar
  7. Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi: 10.1016/j.tree.2008.10.008 CrossRefPubMedGoogle Scholar
  8. Cox DR, Snell EJ (1989) The analysis of binary data, 2nd edn. Chapman & Hall, LondonGoogle Scholar
  9. Craig TP, Itami J, Shantz C et al (2000) The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis. Ecol Entomol 25:7–18CrossRefGoogle Scholar
  10. Cronin JT, Hyland K, Abrahamson WG (2001) The pattern, rate, and range of within-patch movement of a stem-galling fly. Ecol Entomol 26:16–24CrossRefGoogle Scholar
  11. Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331. doi: 10.1146/annurev.en.40.010195.001501 CrossRefGoogle Scholar
  12. Digweed SC (2006) Oviposition preference and larval performance in the exotic birch-leafmining sawfly Profenusa thomsoni. Entomol Exp Appl 120:41–49CrossRefGoogle Scholar
  13. Ellis AM (2008) Incorporating density dependence into the oviposition preference-offspring performance hypothesis. J Anim Ecol 77:247–256CrossRefPubMedGoogle Scholar
  14. Emlen D (1992) Observations of a high altitude population of the sage stem-galling fly Eutreta diana (Diptera: Tephritidae) and its associated parasitoids. J Kans Entomol Soc 65:203–207Google Scholar
  15. Fordyce JA (2003) Aggregative feeding of pipevine swallowtail larvae enhances hostplant suitability. Oecologia 135:250–257CrossRefPubMedGoogle Scholar
  16. Fortin MJ, Dale M (2005) Spatial analysis: a guide for ecologists. Cambridge University Press, New YorkGoogle Scholar
  17. Fournier DA, Skaug HJ, Ancheta J et al (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Method Softw 27:233–249CrossRefGoogle Scholar
  18. Fretwell S, Lucas H (1969) On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–36CrossRefGoogle Scholar
  19. Goeden R (1990) Life history of Eutreta diana (Osten Sacken) on Artemisia tridentata Nuttall in southern California (Diptera: Tephritidae). Pan-Pac Entomol 66:24–32Google Scholar
  20. Gripenberg S, Mayhew P, Parnell M (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecol Lett 13:382–393CrossRefGoogle Scholar
  21. Headrick DH, Goeden R (1998) The biology of nonfrugivorous tephritid fruit flies. Annu Rev Entomol 43:217–241CrossRefPubMedGoogle Scholar
  22. Headrick DH, Goeden R (1999) Behavior of flies in the subfamily Tephritinae. In: Aluja M, Norrbom A (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC, Boca Raton, pp 671–707Google Scholar
  23. Jaenike J (1978) On optimal oviposition behavior in phytophagous insects. Theor Popul Biol 14:350–356CrossRefPubMedGoogle Scholar
  24. Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273CrossRefGoogle Scholar
  25. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994. doi: 10.1111/j.1461-0248.2007.01093.x CrossRefPubMedGoogle Scholar
  26. Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Syst 33:641–664CrossRefGoogle Scholar
  27. Karban R, Shiojiri K, Ishizaki S et al (2013) Kin recognition affects plant communication and defence. Proc R Soc B 280:20123062. doi: 10.1098/rspb.2012.3062 PubMedCentralCrossRefPubMedGoogle Scholar
  28. Levins R, MacArthur R (1969) An hypothesis to explain the incidence of monophagy. Ecology 50:910–911. doi: 10.2307/1933709 CrossRefGoogle Scholar
  29. Mayhew P (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428CrossRefGoogle Scholar
  30. Miller TEX (2007) Demographic models reveal the shape of density dependence for a specialist insect herbivore on variable host plants. J Anim Ecol 76:722–729. doi: 10.1111/j.1365-2656.2007.01239.x CrossRefPubMedGoogle Scholar
  31. Mitchell R (1975) The evolution of oviposition tactics in the bean weevil, Callosobruchus maculatus (F.). Ecology 56:696–702CrossRefGoogle Scholar
  32. Price PW, Cobb N, Craig TP et al (1990) Insect herbivore population dynamics on trees and shrubs: new approaches relevant to latent and eruptive species and life table development. In: Bernays EA (ed) Insect-plant Interactions. CRC, Boca Raton, pp 1–38Google Scholar
  33. Prokopy RJ (1972) Evidence for a marking pheromone deterring repeated oviposition in apple maggot flies. Environ Entomol 1:326–332CrossRefGoogle Scholar
  34. R Core Team (2014) R: A language and environment for statistical computingGoogle Scholar
  35. Roitberg B, Prokopy RJ (1987) Insects that mark host plants. Bioscience 37:400–406CrossRefGoogle Scholar
  36. Sibly R, Barker D, Denham M et al (2005) On the regulation of populations of mammals, birds, fish, and insects. Science 309:607CrossRefPubMedGoogle Scholar
  37. Skaug HJ, Fournier DA, Nielsen A et al (2013) Generalized linear mixed models using AD model builderGoogle Scholar
  38. Thompson J (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14CrossRefGoogle Scholar
  39. Underwood N (2007) Variation in and correlation between intrinsic rate of increase and carrying capacity. Am Nat 169:136–141. doi: 10.1086/509942 CrossRefPubMedGoogle Scholar
  40. Valladares GR, Lawton JH (1991) Host-plant selection in the holly leaf-miner: does mother know best? J Anim Ecol 60:227–240CrossRefGoogle Scholar
  41. Ver Hoef JM, Boveng PL (2007) Quasi-Poisson vs. negative binomial regression: how should we model overdispersed count data? Ecology 88:2766–2772CrossRefPubMedGoogle Scholar
  42. Wetzel WC (2014) Density-dependent recruitment structures a heterogeneous distribution of herbivores among host plants. Ecology 95:2894–2903. doi: 10.1890/14-0190.1 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Evolution and EcologyUniversity of CaliforniaDavisUSA
  2. 2.Department of EntomologyCornell UniversityIthacaUSA

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