Arthropod-Plant Interactions

, Volume 13, Issue 1, pp 99–108 | Cite as

Seasonal assembly of arthropod communities on milkweeds experiencing simulated herbivory

  • Ian S. PearseEmail author
  • Marshall McMunn
  • Louie H. Yang
Original Paper


The seasonal assembly of arthropod communities is shaped by biotic and abiotic aspects of the habitat that limit the appearance or activity phenology of potential community members. In addition, previous interactions within the community, such as herbivore-induced plant defensive responses, aggregation, and predator avoidance likely affect the assembly of arthropod communities on individual plants. We observed the phenology of arthropod communities and defensive plant traits on 100 milkweed (Asclepias eriocarpa) individuals at monthly intervals over a growing season. We experimentally wounded a subset of plants each month (April–August) to observe the effect of simulated added herbivore damage on the seasonal assembly of these arthropod communities. All plant traits and measures of arthropod communities changed over the season. The observed response to experimental leaf damage suggested a trend of induced susceptibility in early months, but not late months. Plants receiving early-season simulated herbivory experienced more subsequent leaf damage than unmanipulated plants. We observed several lagged correlations in our study indicating that blue milkweed beetle (Chrysochus cobaltinus) abundance was lower in months following high natural leaf damage, and that the abundance of a secondary omnivore (Lygaeus kalmii) and total predator abundance tended to follow months with high C. cobaltinus abundance. Ahistorical habitat factors determined much of the observed seasonality of arthropod communities, but induced responses to simulated herbivory also contributed historical effects that influenced arthropod community assembly.


Milkweed Phenology Community assembly Historical contingency Environmental filter Induced responses to herbivory 



We thank Vince Voegeli and the UC Natural Reserves system for access to Hastings Natural History Reserve. Griffin Hall, Lindsay Brandt, Jill Baty, and Sandra Ferguson helped with arthropod surveys. David Zaya provided useful advice on statistics. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. This project was supported in part by a National Science Foundation (NSF) CAREER Grant (DEB-1253101) awarded to LHY. The data and analyses for the study were archived on USGS ScienceBase


  1. Agrawal AA (2004) Resistance and susceptibility of milkweed: competition, root herbivory, and plant genetic variation. Ecology 85:2118–2133CrossRefGoogle Scholar
  2. Agrawal A (2017) Monarchs and milkweed: a migrating butterfly, a poisonous plant, and their remarkable story of coevolution. Princeton University Press, PrincetonCrossRefGoogle Scholar
  3. Agrawal AA, Fishbein M, Jetter R et al (2009) Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol 183:848–867CrossRefGoogle Scholar
  4. Ali JG, Agrawal AA (2014) Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Funct Ecol 28:1404–1412CrossRefGoogle Scholar
  5. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  6. Bazzaz F (1975) Plant species diversity in old-field successional ecosystems in southern Illinois. Ecology 56:485–488CrossRefGoogle Scholar
  7. Belyea LR, Lancaster J (1999) Assembly rules within a contingent ecology. Oikos 86:402–416CrossRefGoogle Scholar
  8. Benbow M, Lewis A, Tomberlin J, Pechal J (2013) Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. J Med Entomol 50:440–450CrossRefGoogle Scholar
  9. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448CrossRefGoogle Scholar
  10. Buckley LB, Nufio CR, Kirk EM, Kingsolver JG (2015) Elevational differences in developmental plasticity determine phenological responses of grasshoppers to recent climate warming. Proc R Soc B 282:20150441CrossRefGoogle Scholar
  11. Chase JM (2003) Community assembly: when should history matter? Oecologia 136:489–498. CrossRefGoogle Scholar
  12. Diamond J (1975) Assembly of species communities. In: Ecology and Evolution of Communities, pp 342–344Google Scholar
  13. Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86CrossRefGoogle Scholar
  14. Dussourd DE (1999) Behavioral sabotage of plant defense: do vein cuts and trenches reduce insect exposure to exudate? J Insect Behav 12:501–515CrossRefGoogle Scholar
  15. Farrell BD (2001) Evolutionary assembly of the milkweed fauna: Cytochrome oxidase I and the age of Tetraopes beetles. Mol Phylogenet Evol 18:467–478CrossRefGoogle Scholar
  16. Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581CrossRefGoogle Scholar
  17. Forkner RE, Marquis RJ, Lill JT (2004) Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol Entomol 29:174–187CrossRefGoogle Scholar
  18. Forrest JR, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491CrossRefGoogle Scholar
  19. Fridley J, Stachowicz J, Naeem S et al (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17CrossRefGoogle Scholar
  20. Halitschke R, Schittko U, Pohnert G et al (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717CrossRefGoogle Scholar
  21. Helmus MR, Dussourd DE (2005) Glues or poisons: which triggers vein cutting by monarch caterpillars? Chemoecology 15:45–49CrossRefGoogle Scholar
  22. Hougen-Eitzman D, Karban R (1995) Mechanisms of interspecific competition that result in successful control of Pacific mites following inoculations of Willamette mites on grapevines. Oecologia 103:157–161CrossRefGoogle Scholar
  23. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994CrossRefGoogle Scholar
  24. Keddy PA (1992) Assembly and response rules: two goals for predictive community ecology. J Veg Sci 3:157–164CrossRefGoogle Scholar
  25. Kraft NJ, Adler PB, Godoy O et al (2015) Community assembly, coexistence and the environmental filtering metaphor. Funct Ecol 29:592–599CrossRefGoogle Scholar
  26. Krimmel BA, Pearse IS (2013) Sticky plant traps insects to enhance indirect defence. Ecol Lett 16:219–224. CrossRefGoogle Scholar
  27. Lawton J, Hassell M (1981) Asymmetrical competition in insects. Nature 289:793–795CrossRefGoogle Scholar
  28. Lill JT, Marquis RJ (2003) Ecosystem engineering by caterpillars increases insect herbivore diversity on white oak. Ecology 84:682–690CrossRefGoogle Scholar
  29. Maire V, Gross N, Börger L et al (2012) Habitat filtering and niche differentiation jointly explain species relative abundance within grassland communities along fertility and disturbance gradients. New Phytol 196:497–509CrossRefGoogle Scholar
  30. Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol Exp Appl 80:193–196CrossRefGoogle Scholar
  31. Martel JW, Malcolm SB (2004) Density-dependent reduction and induction of milkweed cardenolides by a sucking insect herbivore. J Chem Ecol 30:545–561CrossRefGoogle Scholar
  32. McMunn MS (2017) The timing of leaf damage affects future herbivory in mountain sagebrush (Artemisia tridentata). Ecology 98:1996–2002CrossRefGoogle Scholar
  33. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  34. Nufio CR, McGuire CR, Bowers MD, Guralnick RP (2010) Grasshopper community response to climatic change: variation along an elevational gradient. PLoS ONE 5:e12977CrossRefGoogle Scholar
  35. Oksanen J, Blanchet FG, Kindt R et al (2010) vegan: Community Ecology PackageGoogle Scholar
  36. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. CrossRefGoogle Scholar
  37. Piovia-Scott J, Yang LH, Wright AN (2017) Trophic cascades in time: the causes and consequences of temporal variation in the strength of top-down effects. Annu Rev Ecol Evol Syst 48Google Scholar
  38. Polgar CA, Primack RB (2011) Leaf-out phenology of temperate woody plants: from trees to ecosystems. New Phytol 191:926–941CrossRefGoogle Scholar
  39. Quintero C, Lampert EC, Bowers MD (2014) Time is of the essence: direct and indirect effects of plant ontogenetic trajectories on higher trophic levels. Ecology 95:2589–2602CrossRefGoogle Scholar
  40. Rasmann S, Agrawal AA, Cook SC, Erwin AC (2009) Cardenolides, induced responses, and interactions between above- and belowground herbivores of milkweed (Asclepias spp.). Ecology 90:2393–2404CrossRefGoogle Scholar
  41. Roitberg BD, Prokopy RJ (1987) Insects that mark host plants. Bioscience 37:400–406CrossRefGoogle Scholar
  42. Rudolf VH, Armstrong J (2008) Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems. Oecologia 157:675–686CrossRefGoogle Scholar
  43. Shiojiri K, Karban R (2008) Seasonality of herbivory and communication between individuals of sagebrush. Arthropod-Plant Interact 2:87–92. CrossRefGoogle Scholar
  44. Song C, Altermatt F, Pearse IS, Saavedra S (2018) Structural changes within trophic levels are constrained by within-family assembly rules at lower trophic levels. Ecol Lett 21:1221–1228CrossRefGoogle Scholar
  45. Strathdee A, Bale J, Block W et al (1993) Effects of temperature elevation on a field population of Acyrthosiphon svalbardicum (Hemiptera: Aphididae) on Spitsbergen. Oecologia 96:457–465CrossRefGoogle Scholar
  46. Thibault KM, Brown JH (2008) Impact of an extreme climatic event on community assembly. Proc Natl Acad Sci 105:3410–3415CrossRefGoogle Scholar
  47. Van Zandt PA, Agrawal AA (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629CrossRefGoogle Scholar
  48. Wainwright CE, Wolkovich EM, Cleland EE (2012) Seasonal priority effects: implications for invasion and restoration in a semi-arid system. J Appl Ecol 49:234–241CrossRefGoogle Scholar
  49. Wetzel WC, Screen RM, Li I et al (2016) Ecosystem engineering by a gall-forming wasp indirectly suppresses diversity and density of herbivores on oak trees. Ecology 97:427–438CrossRefGoogle Scholar
  50. Wolkovich EM, Cleland EE (2011) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294CrossRefGoogle Scholar
  51. Yang LH (2012) The ecological consequences of insect outbreaks. In: Insect outbreaks revisited. Wiley, Boston, pp 197–218CrossRefGoogle Scholar
  52. Zalucki MP, Malcolm SB, Hanlon CC, Paine TD (2012) First-instar monarch larval growth and survival on milkweeds in southern California: effects of latex, leaf hairs and cardenolides. Chemoecology 22:75–88CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  • Ian S. Pearse
    • 1
    Email author
  • Marshall McMunn
    • 2
  • Louie H. Yang
    • 2
  1. 1.Fort Collins Science CenterU.S. Geological SurveyFt CollinsUSA
  2. 2.Department of Entomology and NematologyUniversity of California, DavisDavisUSA

Personalised recommendations