, Volume 186, Issue 3, pp 869–881 | Cite as

Latitudinal variation in responses of a forest herbivore and its egg parasitoids to experimental warming

  • Mariana Abarca
  • John T. Lill
  • Pablo Frank-Bolton
Global change ecology – original research


Disrupted biotic interactions are a predicted consequence of anthropogenic climate change when interactants differ in the magnitude or direction of phenological responses. Here, we examined the responses to artificial warming of northern, southern and central populations of the eastern tent caterpillar and its hymenopteran egg parasitoids. We subjected egg masses from each region to the typical conditions they experience in their source locality or to a warmer temperature regime, to quantify the effects of simulated warming on their relative phenology, survival and neonate starvation endurance. In addition, we characterized spring heat accumulation and cloud cover at each collection site using 30 years of hourly weather station data. As predicted, degree-day accumulation rates decreased with latitude; however, the mid-latitude site experienced what we predict to be the harshest spring conditions for tent caterpillars: slow heat accumulation combined with thick cloud cover. Remarkably, caterpillars from this site exhibited the largest phenological plasticity, hatching a month earlier under warmer than under typical conditions and doubling caterpillar survival. Survival of caterpillars from all regions was enhanced at warmer temperatures, whereas parasitoid survival was unaffected. The starvation endurance of hatchlings increased under warmer conditions in the central and southern populations only. We show that phenological responses to warming differed between hosts and parasitoids, resulting in a 5-day reduction in the relative phenology of wasps and caterpillars in the northern population. Our findings caution that responses to global warming are likely to be population or region specific and cannot be readily generalized, particularly for wide-ranging organisms.


Baryscapus Chalcidoidea Climate change Malacosoma americanum Phenology Synchrony Tent caterpillars 



This research was generously funded by The Washington Biologist’s Field Club, The Harlan Trust Fund, a PhD fellowship from CONACyT (Consejo Nacional de Ciencia y Tecnología, Mexico), and a George Melendez Wright Climate Change Fellowship, National Park Service (USA) to M. Abarca. We thank R. Oppenheimer, C. Indech D. Salehi, and C. Block for their research assistance. The picture for Fig. 1a was kindly provided by J.A. Ballesteros. M. Gates provided invaluable assistance in identifying the egg parasitoids. We are grateful to G. Heimpel, an anonymous reviewer, and all members of DC-PIG and GW Eco-Evo discussion group for constructive comments on previous versions of this manuscript.

Author contribution statement

MA and JTL conceived and designed the experiments. MA performed the experiments, analyzed the data, and wrote the manuscript. PF compiled and analyzed the climate data. All authors participated in editing the manuscript.

Supplementary material

442_2017_4052_MOESM1_ESM.pdf (121 kb)
Supplementary material 1 (PDF 121 kb)
442_2017_4052_MOESM2_ESM.pdf (199 kb)
Supplementary material 2 (PDF 198 kb)
442_2017_4052_MOESM3_ESM.pdf (258 kb)
Supplementary material 3 (PDF 257 kb)


  1. Abarca M (2016) Phenology of black cherry and eastern tent caterpillars: the impact of global climate change. Doctoral dissertation, George Washington UniversityGoogle Scholar
  2. Abarca M, Lill JT (2015) Warming affects hatching time and early season survival of eastern tent caterpillars. Oecologia 179:901–912CrossRefPubMedGoogle Scholar
  3. Alvi SM, Momoi S (1994) Environmental regulation and geographical adaptation of diapause in Cotesia plutellae (Hymenoptera: Braconidae), a parasitoid of the diamondback moth larvae. Appl Entomol Zool 29:89–95. CrossRefGoogle Scholar
  4. Bale JS, Masters GJ, Hodkinson ID et al (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Chang Biol 8:1–16. CrossRefGoogle Scholar
  5. Battisti A, Stastny M, Netherer S et al (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecol Appl 15:2084–2096. CrossRefGoogle Scholar
  6. Berggren Å, Björkman C, Bylund H, Ayres MP (2009) The distribution and abundance of animal populations in a climate of uncertainty. Oikos 118:1121–1126. CrossRefGoogle Scholar
  7. Berryman AA (1996) What causes population cycles of forest Lepidoptera? Trends Ecol Evol 11:28–32. CrossRefPubMedGoogle Scholar
  8. Bonhomme R (2000) Bases and limits to using “” units. Eur J Agron 13:1–10. CrossRefGoogle Scholar
  9. Brewer AM, Gaston KJ (2003) The geographical range structure of the holly leaf-miner. II. Demographic rates. J Anim Ecol 72:82–93. CrossRefGoogle Scholar
  10. Bryant SR, Thomas CD, Bale JS (2000) Thermal ecology of gregarious and solitary nettle-feeding nymphalid butterfly larvae. Oecologia 122:1–10. CrossRefPubMedGoogle Scholar
  11. Butt C, Quiring D, Hébert C et al (2010) Influence of balsam fir (Abies balsamea) budburst phenology on hemlock looper (Lambdina fiscellaria). Entomol Exp Appl 134:220–226. CrossRefGoogle Scholar
  12. Campbell A, Frazer BD, Gilbert N et al (1974) Temperature requirements of some aphids and their parasites. J Appl Ecol 11:431–438. CrossRefGoogle Scholar
  13. Cayton HL, Haddad NM, Gross K et al (2015) Do growing degree days predict phenology across butterfly species? Ecology 96:1473–1479. CrossRefGoogle Scholar
  14. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122. CrossRefPubMedGoogle Scholar
  15. Dyer LA, Richards LA, Short SA, Dodson CD (2013) Effects of CO2 and temperature on tritrophic interactions. PLoS ONE. Google Scholar
  16. Fitzgerald TD (1995) The tent caterpillars, 1st edn. Cornell University Press, IthacaGoogle Scholar
  17. Fitzgerald TD, Willer DE (1983) Tent-building behavior of the eastern tent caterpillar Malacosoma americanum (Lepidoptera: Lasiocampidae). J Kansas Entomol Soc 56:20–31Google Scholar
  18. Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491CrossRefGoogle Scholar
  19. Fracheboud Y, Luquez V, Björkén L et al (2009) The control of autumn senescence in European aspen. Plant Physiol 149:1982–1991. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Futuyma D, Slatkin M (1983) Coevolution. Sinauer Associates Inc, SunderlandGoogle Scholar
  21. Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495. CrossRefPubMedGoogle Scholar
  22. Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126. CrossRefPubMedGoogle Scholar
  23. Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78(7):2145–2152CrossRefGoogle Scholar
  24. Haynes KJ, Allstadt AJ, Klimetzek D (2014) Forest defoliator outbreaks under climate change: effects on the frequency and severity of outbreaks of five pine insect pests. Glob Chang Biol 20:2004–2018. CrossRefPubMedGoogle Scholar
  25. Heimpel GE, Rosenheim JA, Mangel M (1997) Predation on adult aphytis parasitoids in the field. Oecologia 110:346–352CrossRefPubMedGoogle Scholar
  26. Heimpel GE, Mangel M, Rosenheim JA (1998) Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field. Am Nat 152:273–289. CrossRefPubMedGoogle Scholar
  27. Hodgson JA, Thomas CD, Oliver TH et al (2011) Predicting insect phenology across space and time. Glob Chang Biol 17:1289–1300. CrossRefGoogle Scholar
  28. Hothorn T, Hornik K, van de Wiel MA, Zeileis A (2006) A lego system for conditional inference. Am Stat 60:257–263CrossRefGoogle Scholar
  29. Hunter MD (1992) A variable insect–plant interaction: the relationship between tree budburst phenology and population levels of insect herbivores among trees. Ecol Entomol 16:91–95CrossRefGoogle Scholar
  30. Hunter MD, Mcneil JN (1997) Host–plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology 78:977–986CrossRefGoogle Scholar
  31. IPCC (2014) Climate Change 2014: impacts, adaptation, and vulnerability. Part A: Global and sectoral aspects. Contribution of Working Group II. In: Field CB, Barros VR, Dokken DJ et al (eds) Fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New York, p 688Google Scholar
  32. Jarošík V, Honěk A (2011) Developmental database for phenology models: related insect and mite species have similar thermal requirements. J Econ Entomol 104:1870–1876CrossRefPubMedGoogle Scholar
  33. Kalisz S, Wardle GM (1994) Life history variation in Campanula americana (Campanulaceae): population differentiation. Am J Bot 81:521–527. CrossRefGoogle Scholar
  34. Klapwijk MJ, Chris Gröbler B, Ward K et al (2010) Influence of experimental warming and shading on host–parasitoid synchrony. Glob Chang Biol 16:102–112. CrossRefGoogle Scholar
  35. Laube J, Sparks TH, Estrella N et al (2014) Chilling outweighs photoperiod in preventing precocious spring development. Glob Chang Biol 20:170–182. CrossRefPubMedGoogle Scholar
  36. Liu CL (1926) On some factors of natural control of the eastern tent caterpillar (Malacosoma americana Harris), with notes on the biology of the host. Ph.D. dissertation, Cornell University, Ithaca, NYGoogle Scholar
  37. Moribe Y, Niimi T, Yamashita O, Yaginuma T (2001) Samui, a novel cold-inducible gene, encoding a protein with a BAG domain similar to silencer of death domains (SODD/BAG-4), isolated from Bombyx diapause eggs. Eur J Biochem 268:3432–3442. CrossRefPubMedGoogle Scholar
  38. Neal JW, Chittams JL, Bentz J-A (1997) Spring emergence by larvae of the eastern tent caterpillar a hedge against high risk conditions. Ann Entomol Soc Am 90:596–603CrossRefGoogle Scholar
  39. Olsson K, Agren J (2002) Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria. J Evol Biol 15:983–996. CrossRefGoogle Scholar
  40. Ovaskainen O, Skorokhodova S, Yakovleva M et al (2013) Community-level phenological response to climate change. Proc Natl Acad Sci USA 110:13434–13439. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Chang Biol 13:1860–1872. CrossRefGoogle Scholar
  42. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. CrossRefPubMedGoogle Scholar
  43. Parry D, Goyer RA, Lenhard GJ (2001) Macrogeographic clines in fecundity, reproductive allocation, and offspring size of the forest tent caterpillar Malacosoma disstria. Ecol Entomol 26:281–291. CrossRefGoogle Scholar
  44. R Core T (2013) R: a language and environment for statistical computingGoogle Scholar
  45. Rollinson CR, Kaye MW (2012) Experimental warming alters spring phenology of certain plant functional groups in an early successional forest community. Glob Chang Biol 18:1108–1116. CrossRefGoogle Scholar
  46. Romo CM, Tylianakis JM (2013) Elevated temperature and drought interact to reduce parasitoid effectiveness in suppressing hosts. PLoS ONE. Google Scholar
  47. Segarra-Carmona A, Barbosa P (1983) Nutrient content of four rosaceous hosts and their effects on development and fecundity of the eastern tent caterpillar, Malacosoma americanum (Fab.) (Lepidoptera: Lasiocampidae)’. Can J Zool 61(12):2868–2872CrossRefGoogle Scholar
  48. Stacey L, Roe R, Williams K (1975) Mortality of eggs and pharate larvae of the eastern tent caterpillar, Malacosoma americana (F.) (Lepidoptera : Lasiocampidae). J Kans Soc 48:521–523Google Scholar
  49. Stireman JO, Dyer LA, Janzen DH et al (2005) Climatic unpredictability and parasitism of caterpillars: implications of global warming. Proc Natl Acad Sci USA 102:17384–17387. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, OxfordGoogle Scholar
  51. Tauber MJ, Tauber CA, Nyrop JP, Villani MG (1998) Moisture, a vital but neglected factor in the seasonal ecology of insects: hypotheses and tests of mechanisms. Environ Entomol 27:523–530. CrossRefGoogle Scholar
  52. Thompson J (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  53. Uelmen JA, Lindroth RL, Tobin PC et al (2016) Effects of winter temperatures, spring degree-day accumulation, and insect population source on phenological synchrony between forest tent caterpillar and host trees. For Ecol Manage 362:241–250. CrossRefGoogle Scholar
  54. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc Biol Sci 272:2561–2569. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Visser ME, Holleman LJ (2001) Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc Biol Sci 268:289–294. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Voigt W, Perner J, Davies AJ et al (2003) Trophic levels are differentially sensitive to climate ¨. Ecology 84:2444–2453CrossRefGoogle Scholar
  57. Voigt W, Perner J, Hefin Jones T (2007) Using functional groups to investigate community response to environmental changes: two grassland case studies. Glob Chang Biol 13:1710–1721. CrossRefGoogle Scholar
  58. Wagner D (2005) Caterpillars of Eastern North America. Princeton University Press, PrincetonGoogle Scholar
  59. Walther G-R, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395. CrossRefPubMedGoogle Scholar
  60. Way DA, Montgomery RA (2015) Photoperiod constraints on tree phenology, performance and migration in a warming world. Plant Cell Environ 38:1725–1736. CrossRefPubMedGoogle Scholar
  61. Wu L-H, Hoffmann AA, Thomson LJ (2016) Potential impact of climate change on parasitism efficiency of egg parasitoids: a meta-analysis of Trichogramma under variable climate conditions. Agric Ecosyst Environ 231:143–155. CrossRefGoogle Scholar
  62. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10. CrossRefPubMedGoogle Scholar
  63. Yu H, Luedeling E, Xu J (2010) Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc Natl Acad Sci USA 107:22151–22156. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Zohner CM, Benito BM, Svenning JC, Renner SS (2016) Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants. Nat Clim Chang. Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of BiologyGeorgetown UniversityWashingtonUSA
  2. 2.Department of Biological SciencesThe George Washington UniversityWashingtonUSA
  3. 3.Department of Computer ScienceThe George Washington UniversityWashingtonUSA

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