Population Ecology

, Volume 59, Issue 1, pp 17–27 | Cite as

How do two specialist butterflies determine growth and biomass of a shared host plant?

Original article
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Abstract

Although insect herbivory can modify subsequent quantity and quality of their host plants, change in plant quantity following herbivory has received less attention than plant quality. In particular, little is known about how previous herbivore damage determines plant growth and biomass in an insect species-specific manner. We explored whether herbivore species-specific food demand influences plant growth and biomass. To do this, we conducted a series of experiments and field survey using two specialist butterflies, Sericinus montela and Atrophaneura alcinous, and their host plant, Aristolochia debilis. It is known that A. alcinous larva requires four times more food resources to fulfill its development than S. montela larva. Despite that A. alcinous larvae imposed greater damage on plants than S. montela larvae, plant growth did not differ due to herbivory by these species both in single and multiple herbivory events. On the other hand, total aboveground biomass of the plants was reduced more by A. alcinous than S. montela feeding regardless of the number of herbivory events. Feeding on plants with a history of previous herbivory neither decreased nor increased larval growth. Our results suggest that food demand of the two butterfly species determined subsequent plant biomass, although the plant response may depend on tolerance of the host plant (i.e., ability to compensate for herbivore damage). Such difference in the effects of different herbivore species on host plant biomass is more likely to occur than previously thought, because food demand differs in most herbivore species sharing a host plant.

Keywords

Aristolochia Food demand Herbivory history Plant growth response 

Supplementary material

10144_2016_568_MOESM1_ESM.pdf (267 kb)
Supplementary material 1 (PDF 268 kb)

References

  1. Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500CrossRefGoogle Scholar
  2. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302CrossRefPubMedGoogle Scholar
  3. Ali JG, Agrawal AA (2014) Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Funct Ecol 28:1404–1412CrossRefGoogle Scholar
  4. Baldwin IT, Schmelz EA (1994) Constraints on an induced defense: the role of leaf area. Oecologia 97:424–430CrossRefPubMedGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear Mixed-Effects Models Using Eigen and S4. R package version 1.1-5. http://CRAN.R-project.org/package=lme4. Accessed 22 Jan 2016
  6. Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. Am Nat 127:870–892CrossRefGoogle Scholar
  7. Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161:507–522CrossRefPubMedGoogle Scholar
  8. Damman H (1989) Facilitative interactions between two lepidopteran herbivores of Asimina. Oecologia 78:214–219CrossRefPubMedGoogle Scholar
  9. Del-Val EK, Crawley MJ (2005) Are grazing increaser species better tolerators than decreasers? An experimental assessment of defoliation tolerance in eight British grassland species. J Ecol 93:1005–1016CrossRefGoogle Scholar
  10. Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331CrossRefGoogle Scholar
  11. Dimarco RD, Nice CC, Fordyce JA (2012) Family matters: effect of host plant variation in chemical and mechanical defenses on a sequestering specialist herbivore. Oecologia 170:687–693CrossRefPubMedGoogle Scholar
  12. Erb M, Robert CAM, Hibbard BE, Turlings TCJ (2011) Sequence of arrival determines plant-mediated interactions between herbivores. J Ecol 99:7–15CrossRefGoogle Scholar
  13. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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
  15. Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25:399–407CrossRefGoogle Scholar
  16. Gavloski JE, Lamb RJ (2000) Compensation for herbivory in cruciferous plants: specific responses to three defoliating insects. Environ Entomol 29:1258–1267CrossRefGoogle Scholar
  17. Guillet C, Bergström R (2006) Compensatory growth of fast-growing willow (Salix) coppice in response to simulated large herbivore browsing. Oikos 113:33–42CrossRefGoogle Scholar
  18. Halekoh U, Højsgaard S (2013) pbkrtest: Parametric Bootstrap and Kenward Roger Based Methods for Mixed Model Comparison. R package version 0.3-8. http://CRAN.R-project.org/package=pbkrtest. Accessed 22 Jan 2016
  19. Harrison S, Maron JL (1995) Impacts of defoliation by tussock moths (Orgyia vetusta) on the growth and reproduction of bush lupine (Lupinus arboreus). Ecol Entomol 20:223–229CrossRefGoogle Scholar
  20. Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058CrossRefGoogle Scholar
  21. Hendrix SD (1988) Herbivory and its impact on plant reproduction. In: Doust JL, Doust LL (eds) Plant reproductive ecology: patterns and strategies. Oxford University Press, Oxford, pp 246–263Google Scholar
  22. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994CrossRefPubMedGoogle Scholar
  23. Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347CrossRefGoogle Scholar
  24. Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  25. Kumar V, Poonam, Prasad AK, Parmar VS (2003) Naturally occurring aristolactams, aristolochic acids and dioxoaporphines and their biological activities. Nat Prod Rep 20:565–583CrossRefPubMedGoogle Scholar
  26. Lenth R (2015) lsmeans: least-squares means. R package version 2.15. http://CRAN.R-project.org/package=lsmeans. Accessed 22 Jan 2016
  27. Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539CrossRefPubMedGoogle Scholar
  28. Martinsen GD, Driebe EM, Whitham TG (1998) Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79:192–200CrossRefGoogle Scholar
  29. Massad TJ (2013) Ontogenetic differences of herbivory on woody and herbaceous plants: a meta-analysis demonstrating unique effects of herbivory on the young and the old, the slow and the fast. Oecologia 172:1–10CrossRefPubMedGoogle Scholar
  30. Matsuka H, Ohno Y (1981) An epoch of Sericinus montela. Yadoriga 103(104):15–22 (in Japanese) Google Scholar
  31. McPherson K, Williams K (1998) The role of carbohydrate reserves in the growth, resilience, and persistence of cabbage palm seedlings (Sabal palmetto). Oecologia 117:460–468CrossRefPubMedGoogle Scholar
  32. Miller-Pierce MR, Preisser EL (2012) Asymmetric priority effects influence the success of invasive forest insects. Ecol Entomol 37:350–358CrossRefGoogle Scholar
  33. Mooney EH, Tiedeken EJ, Muth NZ, Niesenbaum RA (2009) Differential induced response to generalist and specialist herbivores by Lindera benzoin (Lauraceae) in sun and shade. Oikos 118:1181–1189CrossRefGoogle Scholar
  34. Mundim FM, Bruna EM, Vieira-Neto EHM, Vasconcelos HL (2012) Attack frequency and the tolerance to herbivory of Neotropical savanna trees. Oecologia 168:405–414CrossRefPubMedGoogle Scholar
  35. Nishida R (1994) Sequestration of plant secondary compounds by butterflies and moths. Chemoecology 138:127–138CrossRefGoogle Scholar
  36. Nishida R, Fukami H (1989) Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly, Atrophaneura alcinous, to aristolochic acids. J Chem Ecol 15:2549–2563CrossRefPubMedGoogle Scholar
  37. Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36:81–105CrossRefGoogle Scholar
  38. Poelman EH, van Loon JJA, Dicke M (2008) Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci 13:534–541CrossRefPubMedGoogle Scholar
  39. Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251CrossRefGoogle Scholar
  40. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  41. Raupp MJ, Denno RF (1983) Leaf age as a predictor of herbivore distribution and abundance. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 91–124CrossRefGoogle Scholar
  42. Rausher MD, Feeny P (1980) Herbivory, plant density, and plant reproductive success: the effect of Battus philenor on Aristolochia reticulata. Ecology 61:905–917CrossRefGoogle Scholar
  43. Ritchie ME, Tilman D (1992) Interspecific competition among grasshoppers and their effect on plant abundance in experimental field environments. Oecologia 89:524–532CrossRefPubMedGoogle Scholar
  44. Sakuratani Y, Kanno K (2003) Seasonal changes of Sericinus montela on the bank of Kizu River in Kyoto prefecture with special reference to comparison to Atrophaneura alcinous. In: Sunose T, Eda K (eds) Decline and conservation of butterflies in Japan, V. Lepidopterological Society of Japan, Tokyo, pp 181–184 (in Japanese) Google Scholar
  45. Sakuratani Y, Kanno K, Michioka Y (2003) Interspecific interaction between native butterfly Atrophaneura alcinous and exotic butterfly Sericinus montela. In: Kizu River Research Group, River Ecology Research Group of Japan (eds) Comprehensive studies on Kizu River. Riverfront Improvement and Restoration, Tokyo, pp 381–398 (in Japanese) Google Scholar
  46. Shoji Y (1997) Sericinus montela, an introduced butterfly. In: Ishii M, Johki Y, Ohtani T (eds) The encyclopedia of animals in Japan. No. 9. Heibonsha Limited, Publishers, Tokyo, p 33 (in Japanese) Google Scholar
  47. Suzuki N (1998) Analysis of interaction between Aristolochia debilis with vigorous chemical defenses and phytophagous insects. Report of the Grant-in-Aid for Scientific Research (no. 07640848) by Ministry of Education, Science, Sports and Culture (in Japanese) Google Scholar
  48. Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536CrossRefGoogle Scholar
  49. Underwood N (2000) Density dependence in induced plant resistance to herbivore damage: threshold, strength and genetic variation. Oikos 89:295–300CrossRefGoogle Scholar
  50. Underwood N (2012) When herbivores come back: effects of repeated damage on induced resistance. Funct Ecol 26:1441–1449CrossRefGoogle Scholar
  51. Utsumi S, Ando Y, Ohgushi T (2009) Evolution of feeding preference in a leaf beetle: the importance of phenotypic plasticity of a host plant. Ecol Lett 12:920–929CrossRefPubMedGoogle Scholar
  52. Utsumi S, Ando Y, Roininen H, Takahashi J, Ohgushi T (2013) Herbivore community promotes trait evolution in a leaf beetle via induced plant response. Ecol Lett 16:362–370CrossRefPubMedGoogle Scholar
  53. Van Zandt PA, Agrawal AA (2004) Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca. Oikos 104:401–409CrossRefGoogle Scholar
  54. Viswanathan DV, Narwani AJT, Thaler JS (2005) Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–896CrossRefGoogle Scholar
  55. Viswanathan DV, Lifchits OA, Thaler JS (2007) Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–1399CrossRefGoogle Scholar

Copyright information

© The Society of Population Ecology and Springer Japan 2016

Authors and Affiliations

  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan

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