Oecologia

, Volume 152, Issue 2, pp 365–375 | Cite as

Extreme weather change and the dynamics of oviposition behavior in the pipevine swallowtail, Battus philenor

  • Daniel R. Papaj
  • Heather S. Mallory
  • Cheryl A. Heinz
Behavioral Ecology

Abstract

Prospects of global increases in extreme weather change provide incentive to examine how such change influences animal behavior, for example, behavior associated with resource use. In this study, we examined how oviposition behavior in a southern Arizona population of pipevine swallowtails (Battus philenor L.) responded to changes in their Aristolochia host resource and vegetative background caused by the North American monsoon system. Summer monsoon rains resulted in a flush of non-host vegetation and a more than doubling in rate of landings by host-searching females on non-host vegetation. Rates of discovery of the host species A. watsoni Woot. Standl. decreased by 50% after monsoon rains. Rains did not alter host density appreciably, but resulted in significant increases in host plant size and new growth, two indicators of host suitability for B. philenor larvae. After the rains, mean clutch size on individual host plants increased by a factor of 2.5; the mean proportion of host plants encountered on which a female laid eggs also increased significantly. Females were discriminating about the host plants on which they laid eggs after alightment; plants accepted for oviposition were larger, bore more new growth, and bore fewer larvae than rejected plants. Contrary to predictions from foraging theory, degree of discrimination did not change seasonally. Finally, the rate at which eggs were laid increased seasonally, suggesting that oviposition rates were limited more before monsoon rains by the relatively low quality of hosts than they were after the rains by the relatively low rate at which hosts were found. This latter result suggests that, while butterflies possess behavioral flexibility to respond to extreme weather change, such flexibility may have limits. In particular, expected increases in the severity and frequency of droughts may result in reduced oviposition rates, reductions that could have adverse demographic consequences.

Keywords

Climate change Host selection Egg load Clutch size Butterfly 

Notes

Acknowledgements

Thanks to Joshua Garcia, Laura Mojonnier, and Ginny Newsom for field assistance, and to the Papaj lab group for discussions. We acknowledge helpful comments by J. Rosenheim and two anonymous reviewers. Funding was provided by the National Science Foundation (award no. IBN0112067). C. Heinz was funded by the Center for Insect Science through an NIH award (no. 1K12Gm00708). We are grateful to Mark Heitlinger and the SRER Executive Committee for permission to work on the Santa Rita Experimental Range, and to Bill Emmerich for rain gauge data.

References

  1. Adams DK, Comrie AC (1997) The North American monsoon. Bull Am Meteorol Soc 78:2197–2213CrossRefGoogle Scholar
  2. Bazzaz FA (1998) Tropical forests in a future climate: changes in biological diversity and impact on the global carbon cycle. Clim Change 39:317–336CrossRefGoogle Scholar
  3. Bolger DT, Patten MA, Bostock DC (2005) Avian reproductive failure in response to an extreme climatic event. Oecologia 142:398–406PubMedCrossRefGoogle Scholar
  4. Coley PD (1998) Possible effects of climate change on plant/herbivore interactions in moist tropical forests. Clim Change 39:455–472CrossRefGoogle Scholar
  5. Easterling DR, Changnon S, Karl TR, Meehl J, Parmesan C (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074PubMedCrossRefGoogle Scholar
  6. Ellis AW, Saffell EM, Hawkins TW (2004) A method for defining monsoon onset and demise in the southwestern USA. Int J Climatol 24:247–265CrossRefGoogle Scholar
  7. Feeny P (1976) Plant apparency and chemical defense. Rec Adv Phytochem 10:1–40Google Scholar
  8. Fordyce JA (2000) A model without a mimic: aristolochic acids from the California pipevine swallowtail, Battus philenor hirsuta, and its host plant, Aristolochia californica. J Chem Ecol 26:2567–2578CrossRefGoogle Scholar
  9. Fordyce JA (2001) The lethal plant defense paradox remains: inducible host-plant aristolochic acids and the growth and defense of the pipevine swallowtail. Entomol Exp Appl 100:339–346CrossRefGoogle Scholar
  10. Fordyce JA (2003) Aggregative feeding of pipevine swallowtail larvae enhances hostplant suitability. Oecologia 135:250–257PubMedGoogle Scholar
  11. Fordyce JA, Nice CC (2003) Contemporary patterns in a historical context: phylogeographic history of the pipevine swallowtail, Battus philenor (Papilionidae). Evolution 57:1089–1099PubMedCrossRefGoogle Scholar
  12. Fordyce JA, Nice CC (2004) Geographic variation in clutch size and a realized benefit of aggregative feeding. Evolution 58:447–450PubMedCrossRefGoogle Scholar
  13. IPCC (Intergovernmental Panel on Climate Change) (2001) Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (eds) Climate change 2001: the science of climate change, contribution of Working Group I to the Intergovernmental Panel on Climate Change third assessment report. Cambridge University Press, CambridgeGoogle Scholar
  14. Johns CV, Hughes A (2002) Interactive effects of elevated CO2 and temperature on the leaf-miner Dialectica scalariella Zeller (Lepidoptera: Gracillariidae) in Paterson’s curse, Echium plantagineum (Boraginaceae). Global Change Biol 8:142–152CrossRefGoogle Scholar
  15. Karl TR, Knight RW, Plummer N (1995) Trends in high-frequency climate variability in the 20th century. Nature 377:217–220CrossRefGoogle Scholar
  16. Knapp AK, Fay PA, Blair JM, Collins SL, Smith MD, Carlisle JD, Harper CW, Danner BT, Lett MS, McCarron JK (2002) Rainfall variability, carbon, cycling, and plant species diversity in a mesic grassland. Science 298:2202–2205PubMedCrossRefGoogle Scholar
  17. Mangel M (1987) Oviposition site selection and clutch size in insects. J Math Biol 25:1–22CrossRefGoogle Scholar
  18. Mangel M (1989) An evolutionary interpretaton of the “motivation to oviposit”. J Evol Biol 2:157–172CrossRefGoogle Scholar
  19. McLaughlin JF, Hellmann JJ, Boggs CL, Ehrlich PR (2002) Climate change hastens population extinctions. Proc Natl Acad Sci USA 99:6070–6074PubMedCrossRefGoogle Scholar
  20. Meehl GA, Zwiers F, Evans J, Knutson T, Mearns L, Whetton P (2000) Trends in extreme weather and climate events: issues related to modeling extremes in projections of future climate change. Bull Am Meteorol Soc 81:427–436CrossRefGoogle Scholar
  21. Minkenberg OPJM, Tatar M, Rosenheim JA (1992) Egg load as a major source of variability in insect foraging and oviposition behavior. Oikos 65:134–142CrossRefGoogle Scholar
  22. Odendaal FJ, Rausher MD (1990) Eggload influences host search intensity, host preference, and clutch size in Battus philenor (Papilionidae). J Insect Behav 3:183–193CrossRefGoogle Scholar
  23. Papaj DR (1986a) Leaf buds, a factor in host selection by Battus philenor butterflies. Ecol Entomol 11:301–307Google Scholar
  24. Papaj DR (1986b) Shifts in foraging behavior by a Battus philenor population: field evidence for switching by individual butterflies. Behav Ecol Sociobiol 19:31–39CrossRefGoogle Scholar
  25. Papaj DR (1990) Interference with learning in pipevine swallowtail butterflies: behavioural constraint or possible adaptation? Symp Biol Hung 39:89–101Google Scholar
  26. Papaj DR, Newsom GM (2005) A within-species warning function for an aposematic signal. Proc R Soc Lond 272:2519–2523CrossRefGoogle Scholar
  27. Papaj DR, Rausher MD (1987) Components of conspecific host discrimination behavior in the butterfly Battus philenor. Ecology 68:245–253CrossRefGoogle Scholar
  28. Parmesan C (1996) Climate and species’ range. Nature 382:765–766CrossRefGoogle Scholar
  29. Parmesan C (2001) Coping with modern times? Insect movement and climate change. In: Woiwod I, Reynolds DR, Thomas CD (eds) Insect movement: mechanisms and consequences. CAB International, WallingfordGoogle Scholar
  30. Parmesan C, Galbraith H (2004) Observed impacts of global climate change in the US. Prepared for Pew Center on Global Climate ChangeGoogle Scholar
  31. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42PubMedCrossRefGoogle Scholar
  32. Pilson D, Rausher MD (1988) Clutch size adjustment by a swallowtail butterfly. Nature 333:361–363CrossRefGoogle Scholar
  33. Rausher MD (1978) Search image for leaf shape in a butterfly. Science 200:1071–1073CrossRefGoogle Scholar
  34. Rausher MD (1979) Egg recognition: its advantage to a butterfly. Anim Behav 27:1034–1040CrossRefGoogle Scholar
  35. Rausher MD (1980) Host abundance, juvenile survival, and oviposition preference in Battus philenor. Evolution 34:342–355CrossRefGoogle Scholar
  36. Rausher MD (1981a) Host plant selection by Battus philenor butterflies: the roles of predation, nutrition, and plant chemistry. Ecol Monographs 51:1–20CrossRefGoogle Scholar
  37. Rausher MD (1981b) The effect of native vegetation on the susceptibility of Aristolochia reticulata (Aristolochiaceae) to herbivore attack. Ecology 62:1187–1195CrossRefGoogle Scholar
  38. Rausher MD (1983) Alteration of oviposition behavior by Battus philenor butterflies in response to variation in host-plant density. Ecology 64:1028–1034CrossRefGoogle Scholar
  39. Rausher MD, Papaj DR (1983) Demographic consequences of discrimination among conspecific host plants by Battus philenor butterflies. Ecology 64:1402–1410CrossRefGoogle Scholar
  40. Roitberg B, Sircom J, Roitberg C, van Alphen J, Mangel M (1993) Life expectancy and reproduction. Nature 364:108PubMedCrossRefGoogle Scholar
  41. Rubenstein DI (1992) The greenhouse effect and changes in animal behavior: effects on social structure and life history strategies. In: Peters RL, Lovejoy TE (eds) Global warming and biological diversity. Yale University Press, New Haven, Conn.Google Scholar
  42. SAS (2000) JMP-IN, version 4. SAS Institute, Cary, N.C.Google Scholar
  43. Sime KR (2002) Chemical defense of Battus philenor larvae against attack by the parasitoid Trogus pennator. Ecol Entomol 27:337–345CrossRefGoogle Scholar
  44. Sime KR, Feeny PP, Haribal MM (2000) Sequestration of aristolochic acids by the pipevine swallowtail, Battus philenor (L): evidence and ecological implications. Chemoecology 10:169–178CrossRefGoogle Scholar
  45. Snell-Rood EC, Papaj DR (2006) Learning signals within sensory environments: Does host cue learning in butterflies depend on background? Anim Biol 56:173–192CrossRefGoogle Scholar
  46. Tatar M (1991) Clutch size in the swallowtail butterfly, Battus philenor: the role of host quality and egg load within and among seasonal flights in California. Behav Ecol Sociobiol 28:337–344CrossRefGoogle Scholar
  47. Veteli TO, Kuokkanen K, Julkunen-Tiitto R, Roininen R, Tahvanainen J (2002) Effects of elevated CO2 and temperature on plant growth and herbivore defensive chemistry. Global Change Biol 8:1240–1252CrossRefGoogle Scholar
  48. Warren JM, Bassman JH, Eigenbrode S (2002) Leaf chemical changes induced in Populus trichocarpa by enhanced UV-B radiation and concomitant effects on herbivory by Chrysomela scripta (Coleoptera: Chrysomelidae). Tree Physiol 22:1137–1146PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Daniel R. Papaj
    • 1
  • Heather S. Mallory
    • 1
    • 2
  • Cheryl A. Heinz
    • 1
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.Department of BiologyGeorgetown UniversityWashingtonUSA
  3. 3.Department of BiologyBenedictine UniversityLisleUSA

Personalised recommendations