Skip to main content
Springer Nature Link
Log in

Host plant limitation of butterflies in highly fragmented landscapes

  • Original Paper
  • Published:
Theoretical Ecology Aims and scope Submit manuscript

Abstract

Insect herbivores can be limited by host plants in two ways: density-dependent competition for food resources or density-independent search time limitation. Our understanding of density-dependent host plant limitation is relatively well developed and well integrated into conservation plans for at-risk insects. Search time limitation, a density-independent process, is much less well developed. Here, we explore both mechanisms using empirically based models of monarch butterfly population dynamics. These mechanisms differ fundamentally in their predictions: resource competition leads to matching of herbivore densities to host plant densities, and visible competition via consumption of host plants. Search time limitation leads to changes in population growth rate that can cause herbivore numbers to decline when host plant densities are constant. Search time limitation also implies that host plants can limit herbivores, even when many individual plants are uneaten. For monarch butterflies, our calculations suggest that many parts of North America have host plant densities below the threshold for search time limitation, which contrasts with the typical assumption of resource competition. More generally, incorporating search time limitation into conservation plans is important for reframing our understanding of how host plants limit insect herbivores in highly fragmented landscapes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and material

Not applicable.

Code availability

Included for review.

References

  • Agrawal AA (2019) Advances in understanding the long-term population decline of monarch butterflies. Proc Natl Acad Sci 116(17):8093–8095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altizer SM, Oberhauser KS (1999) Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). J Invertebr Pathol 74:76–88

    Article  CAS  PubMed  Google Scholar 

  • Ballew AM (2021) Effects of nectar and infection on flight performance and fitness in monarchs (Masters thesis, University of Georgia). https://www.proquest.com/docview/2571013282 Accessed 20 Nov 2021

  • Barnay O, Pizzol J, Gertz C, Kienlen JC, Hommay G, Lapchin L (1999) Host density-dependence of discovery and exploitation rates of egg patches of Lobesia botrana (Lepidoptera: Tortricidae) and Ephestia kuehniella (Lepidoptera: Pyralidae) by the Parasitoid Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). J Econ Entomol 92:1311–1320

    Article  Google Scholar 

  • Belovsky GE (1978) Diet optimization in a generalist herbivore, the moose. Theor Popul Biol 14:105–134

    Article  CAS  PubMed  Google Scholar 

  • Belovsky GE (1984) Herbivore optimal foraging: a comparative test of 3 models. Am Nat 124:97–115

    Article  Google Scholar 

  • Borkin SS (1982) Notes on shifting distribution patterns and survival of immature Danuas plexippus (Lepidoptera, Danaidae) on the food plant Asclepias syriaca. Great Lakes Entomol 15:199–206

    Google Scholar 

  • Brown LM, Fuda RK, Schtickzelle N, Coffman H, Jost A, Kazberouk A, Kemper E et al (2017) Using animal movement behavior to categorize land cover and predict consequences for connectivity and patch residence times. Landscape Ecol 32:1657–1670

    Article  Google Scholar 

  • Caswell H (2001) Matrix population models: construction, analysis, and interpretation. Sunderland, Mass, Sinauer Associates

  • Caswell H, Neubert MG, Hunter CM (2011) Demography and dispersal: invasion speeds and sensitivity analysis in periodic and stochastic environments. Thyroid Res 4:407–421

    Google Scholar 

  • Crone EE, Brown LM, Hodgson JA, Lutscher F, Schultz CB (2019) Faster movement in nonhabitat matrix promotes range shifts in heterogeneous landscapes. Ecology 100

  • Crone EE, Schultz CB (2021) Resilience or catastrophe? A possible state change for monarch butterflies in western North America. Ecol Lett 24:1533–1538

    Article  PubMed  Google Scholar 

  • Dempster J (1983) The natural control of populations of butterflies and moths. Biol Rev 58:461–481

    Article  Google Scholar 

  • Dennis R, Shreeve TG, Van Dyck H (2003) Towards a functional resource-basec concept for habitat: a butterfly biology viewpoint. Oikos 102:417–426

    Article  Google Scholar 

  • Doak P, Kareiva P, Kingsolver J (2006) Fitness consequences of choosy oviposition for a time-limited butterfly. Ecology 87:395–408

    Article  PubMed  Google Scholar 

  • Ewen JG, Walker L, Canessa S, Groombridge JJ (2015) Improving supplementary feeding in species conservation. Conserv Biol 29:341–349

    Article  PubMed  Google Scholar 

  • Fahrig L, Paloheimo J (1988) Effect of spatial arrangement of habitat patches on local population size. Ecology 69:468–475

    Article  Google Scholar 

  • Fisher KE, Adelman JS, Bradbury SP (2020) Employing very high frequency (VHF) radio telemetry to recreate monarch butterfly flight paths. Environ Entomol 49:312–323

    Article  PubMed  Google Scholar 

  • Flockhart DTT, Martin TG, Norris DR (2012) Experimental examination of intraspecific density-dependent competition during the breeding period in monarch butterflies (Danaus plexippus). Plos One 7

  • Flockhart DTT, Pichancourt J-B, Norris DR, Martin TG (2015) Unravelling the annual cycle in a migratory animal: breeding-season habitat loss drives population declines of monarch butterflies. J Anim Ecol 84:155–165

    Article  PubMed  Google Scholar 

  • Flockhart DTT, Wassenaar LI, Martin TG, Hobson KA, Wunder MB, Norris MB (2013) Tracking multi-generational colonization of the breeding grounds by monarch butterflies in eastern North America. Proc Royal Soc B 280

  • Hanski I, Ovaskainen O (2002) Extinction debt at extinction threshold. Conserv Biol 16:666–673

    Article  Google Scholar 

  • Hartzler RG (2010) Reduction in common milkweed (Asclepias syriaca) occurrence in Iowa cropland from 1999 to 2009. Crop Prot 29:1542–1544

    Article  Google Scholar 

  • Hassell MP, May R (1974) Aggregation of predators and insect parasites and its effect on stability. J Anim Ecol 567–594

  • Hassell MP, Southwood TRE (1978) Foraging strategies of insects. Annu Rev Ecol Syst 9:75–98

    Article  Google Scholar 

  • Heads PA, Lawton JH (1983) Studies on the natural enemy complex of the holly leaf-miner: the effects of scale on detection of aggregative responses and implications for biological-control. Oikos 40:267–276

    Article  Google Scholar 

  • Holmes EE, Lewis MA, Banks JE, Veit RR (1994) Partial differential equations in ecology: spatial interactions and population dynamics. Ecology 75:17–29

    Article  Google Scholar 

  • Howell PE, Muths E, Hossack BR, Sigafus BH, Chandler RB (2018) Increasing connectivity between metapopulaiton ecology and landscape ecology. Ecology 99:1119–1128

    Article  PubMed  Google Scholar 

  • James DG, James TS, Seymour L, Kappen L, Russell T, Harryman B, Bly C (2018) Citizen scientist tagging reveals destinations of migrating monarch butterflies, Danaus plexippus (L.) from the Pacific Northwest. J Lepid Soc 72:127–144

    Google Scholar 

  • Johansson J, Bergström A, Janz N (2007) The benefit of additional oviposition targets for a polyphagous butterfly. J Insect Sci 7:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnston MK, Hasle EM, Klinger KR, Lambruschi MP, Derby Lewis A, Stotz DF, Winter AM et al (2019) Estimating milkweed abundance in metropolitan areas under existing and user-defined scenarios. Front Ecol Evol 7:210

    Article  Google Scholar 

  • Jones PL, Agrawal AA (2019) Beyond preference and performance: host plant selection by monarch butterflies, Danaus plexippus. Oikos 128:1092–1102

    Article  Google Scholar 

  • Jones R, Gilbert N, Guppy M, Nealis V (1980) Long-distance movement of Pieris rapae. J Anim Ecol 49:629–642

    Article  Google Scholar 

  • Kareiva P (1983) Influence of vegetation texture on herbivore populations: resource concentration and herbivore movement, Pages 259–289 Variable plants and herbivores in natural and managed systems. New York, Academic Press Inc

  • Kareiva P, Odell G (1987) Swarms of predators exhibit preytaxis if individual predators use area-restricted search. Am Nat 130:233–270

    Article  Google Scholar 

  • Kuefler D, Hudgens B, Haddad NM, Morris WF, Thurgate N (2010) The conflicting role of matrix habitats as conduits and barriers for dispersal. Ecology 91:944–950

    Article  PubMed  Google Scholar 

  • Kuussaari M, Bommarco R, Heikkinen RK, Helm A, Krauss J, Lindborg R, Öckinger E et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571

    Article  PubMed  Google Scholar 

  • Lessells CM (1985) Parasitoid foraging: should parasitism be density-dependent? J Anim Ecol 54:27–41

    Article  Google Scholar 

  • Li C, Roitberg B, Mackauer M (1997) Effects of contact kairomone and experience on initial giving-up time. Entomol Exp Appl 84:101–104

    Article  Google Scholar 

  • Lopez-Bao JV, Palomares F, Rodriguez A, Delibes M (2010) Effects of food supplementation on home-range size, reproductive success, productivity and recruitment in a small population of Iberian lynx. Anim Conserv 13:35–42

    Article  Google Scholar 

  • Mac Arthur R, Pianka E (1966) On optimal use of a patchy environment. Amer Natur 100:603–609

    Article  Google Scholar 

  • Marini L, Zalucki MP (2017) Density-dependence in the declining population of the monarch butterfly. Sci Rep 7:1–8

    Article  CAS  Google Scholar 

  • McIntire EJB, Schultz CB, Crone EE (2007) Designing a network for butterfly habitat restoration: where individuals, populations and landscapes interact. J Appl Ecol 44:725–736

    Article  Google Scholar 

  • McKnight S (2016) Monarch and milkweed surveys in the Great Basin: 2016 field season summary. The Xerces Society for Invertebrate Conservation

  • Mills NJ, Heimpel GE (2018) Could increased understanding of foraging behavior help to predict the success of biological control? Curr Opin Insect Sci 27:26–31

    Article  PubMed  Google Scholar 

  • Musgrave JA, Lutscher F (2014) Integrodifference equations in patchy landscapes II. Population level consequences. J Math Biol 69:617–658

    Article  PubMed  Google Scholar 

  • Nagano CD, Sakai WH, Malcolm SB, Cockrell BJ, Brower LP (1993) Spring migration of monarch butterflies in California, Pages 219–232 in S. Malcom, and M. P. Zalucki, eds. Biology and Conservation of Monarch Butterfly. Los Angeles, Natural History Museum of Los Angeles County

  • Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci 105:19052–19059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Brien DM, Boggs CL, Fogel ML (2004) Making eggs from nectar: the role of life history and dietary carbon turnover in butterfly reproductive resource allocation. Oikos 105:279–291

    Article  CAS  Google Scholar 

  • Ovaskainen O, Crone EE (2009) Modeling animal movement with diffusion in S. Cantrell, C. Cosner, and S. Ruan, eds. Spatial Ecology, Chapman and Hall/CRC Press

  • Pelton EM, Schultz CB, Jepsen SJ, Black SH, Crone EE (2019) Western monarch population plummets: status, probable causes, and recommended conservation actions. Front Ecol Evol 7:Article 258

  • Pleasants J (2017) Milkweed restoration in the Midwest for monarch butterfly recovery: estimates of milkweeds lost, milkweeds remaining and milkweeds that must be added to increase the monarch population. Insect Conserv Divers 10:42–53

    Article  Google Scholar 

  • Pleasants JM, Oberhauser KS (2013) Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population. Insect Conserv Divers 6:135–144

    Article  Google Scholar 

  • Pocius VM, Debinski DM, Pleasants JM, Bidne KG, Hellmich RL, Brower LP (2017) Milkweed matters: monarch butterfly (Lepidoptera: Nymphalidae) survival and development on nine Midwestern milkweed species. Environ Entomol 46:1098–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pocius VM, Pleasants JM, Debinski DM, Bidne KG, Hellmich RL, Bradbury SP, Blodgett SL (2018) Monarch butterflies show differential utilization of nine Midwestern milkweed species. Front Ecol Evol 6:169

    Article  Google Scholar 

  • Powell JA, Zimmermann NE (2004) Multiscale analysis of active seed dispersal contributes to resolving Reid’s paradox. Ecology 85:490–506

    Article  Google Scholar 

  • Pyke GH (1984) Optimal foragint theory — a critical review. Annu Rev Ecol Syst 15:523–575

    Article  Google Scholar 

  • Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q R Biol 52:137–154

    Article  Google Scholar 

  • Ries L, Debinski DM (2001) Butterfly responses to habitat edges in the highly fragmented prairies of Central Iowa. J Anim Ecol 70:840–852

    Article  Google Scholar 

  • Ruffino L, Salo P, Koivisto E, Banks PB, Korpimaki E (2014) Reproductive responses of birds to experimental food supplementation: a meta-analysis. Front Zool 11

  • Schultz CB, Crone EE (2001) Edge-mediated dispersal behavior in a prairie butterfly. Ecology 82:1879–1892

    Article  Google Scholar 

  • Schultz CB, Dlugosch KM (1999) Nectar and hostplant scarcity limit populations of an endangered Oregon butterfly. Oecologia 119:231–238

    Article  PubMed  Google Scholar 

  • Shigesada N, Kawasaki K, Teramoto E (1986) Traveling periodic waves in heterogeneous environments. Theor Popul Biol 30:143–160

    Article  Google Scholar 

  • Stiling PD (1987) The frequency of density dependence in insect host-parasitoid systems. Ecology 68:844–856

    Article  Google Scholar 

  • Thogmartin WE, Lopez-Hoffman L, Rohweder J, Diffendorfer J, Drum R, Semmens D, Black S et al (2017a) Restoring monarch butterfly habitat in the Midwestern US: all hands on deck. Environ Res Lett 12

  • Thogmartin WE, Wiederholt R, Oberhauser K, Drum RG, Diffendorfer JE, Altizer S, Taylor SR et al (2017b) Monarch butterfly population decline in North America: identifying the threatening processes. R Soc Open Sci 4

  • Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66

    Article  Google Scholar 

  • US Fish and Wildlife Service (2020) U.S. Fish and Wildlife Service finds Endangered Species Act listing for monarch butterfly warranted but precluded. https://www.fws.gov/news/ShowNews.cfm?ref=u.s.-fish-and-wildlife-service-finds-endangered-species-act-listing-for-&_ID=36817. Accessed 1 Feb 2022

  • Waage JK (1979) Foraging for patchily-distributed hosts by the parasitoid, Nemeritis canescens. J Anim Ecol 48:353–371

    Article  Google Scholar 

  • Wajnberg É (2006) Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms. Behav Ecol Sociobiol 60:589–611

    Article  Google Scholar 

  • Waterbury B, Potter A, Svancara LK (2019) Monarch butterfly distribution and breeding ecology in Idaho and Washington. Front Ecol Evol 7:172

  • Yakubu A-A, Sáenz R, Stein J, Jones LE (2004) Monarch butterfly spatially discrete advection model. Math Biosci 190:183–202

    Article  PubMed  Google Scholar 

  • Yang LH, Cenzer ML (2020) Seasonal windows of opportunity in milkweed–monarch interactions. Ecology 101:e02880

  • Zalucki MP, Kitching RL (1982a) The analysis and description of movement in adult Danaus plexippus L. (Lepidoptera: Danainae). Behaviour 80:174–198

    Article  Google Scholar 

  • Zalucki MP, Kitching RL (1982b) Dynamics of oviposition in Danaus plexippus (Insecta: Lepidoptera) on milkweed Asclepias spp. J Zool 198:103–116

    Article  Google Scholar 

  • Zalucki MP, Parry HR, Zalucki JM (2016) Movement and egg laying in monarchs: to move or not to move, that is the equation. Austral Ecol 41:154–167

    Article  Google Scholar 

  • Zylstra ER, Ries L, Neupane N, Saunders SP, Ramírez MI, Rendón-Salinas E, Oberhauser KS et al (2021) Changes in climate drive recent monarch butterfly dynamics. Nat Ecol Evol 1–12

Download references

Funding

This work benefitted from NSF DEB 1920834 to EEC and CBS and DOD Legacy awards NR 17–836 and NR 19–001 to CBS and EEC.

Author information

Authors and Affiliations

  1. Department of Biology, Tufts University, 200 College Avenue, Medford, MA, 02155, USA

    Elizabeth E. Crone

  2. School of Biological Sciences, Washington State University, 14204 Northeast Salmon Creek Avenue, Vancouver, WA, 98686, USA

    Cheryl B. Schultz

Authors
  1. Elizabeth E. Crone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheryl B. Schultz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elizabeth E. Crone.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crone, E.E., Schultz, C.B. Host plant limitation of butterflies in highly fragmented landscapes. Theor Ecol 15, 165–175 (2022). https://doi.org/10.1007/s12080-021-00527-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12080-021-00527-5

Keywords

Search

Navigation