Skip to main content
SpringerLink
Log in

Losing a battle but winning the war: moving past preference–performance to understand native herbivore–novel host plant interactions

  • Population ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Introduced plants can positively affect population viability by augmenting the diet of native herbivores, but can negatively affect populations if they are subpar or toxic resources. In organisms with complex life histories, such as insects specializing on host plants, the impacts of a novel host may differ across life stages, with divergent effects on population persistence. Most research on effects of novel hosts has focused on adult oviposition preference and larval performance, but adult preference may not optimize offspring performance, nor be indicative of host quality from a demographic perspective. We compared population growth rates of the Baltimore checkerspot butterfly, Euphydryas phaeton, on an introduced host, Plantago lanceolata (English plantain), and the native host Chelone glabra (white turtlehead). Contrary to the previous findings suggesting that P. lanceolata could be a population sink, we found higher population growth rates (λ) on the introduced than the native host, even though some component parameters of λ were higher on the native host. Our findings illustrate the importance of moving beyond preference–performance studies to integrate vital rates across all life stages for evaluating herbivore–host plant relationships. Single measures of preference or performance are not sufficient proxies for overall host quality nor do they provide insights into longer term consequences of novel host plant use. In our system, in particular, P. lanceolata may buffer checkerspot populations when the native host is limiting, but high growth rates could lead to crashes over longer time scales.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Bates D, Maechler M, Bolker B, Walker S (2014) Package Lme4: linear mixed-effects models using Eigen and S4. J Stat Softw 67

  • Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Bezemer TM, Harvey JA, Cronin JT (2014) Response of native insect communities to invasive plants. Annu Rev Entomol 59:119–141

    Article  CAS  PubMed  Google Scholar 

  • Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Boggs CL, Freeman KD (2005) Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144:353–361

    Article  PubMed  Google Scholar 

  • Boggs CL, Ross CL (1993) The effect of adult food limitation on life-history traits in Speyeria mormonia (Lepidoptera, Nymphalidae). Ecology 74:433–441

    Article  Google Scholar 

  • Boggs CL et al (2006) Delayed population explosion of an introduced butterfly. J Anim Ecol 75:466–475

    Article  PubMed  Google Scholar 

  • Boughton DA (1999) Empirical evidence for complex source–sink dynamics with alternative states in a butterfly metapopulation. Ecology 80:2727–2739

    Google Scholar 

  • Boughton DA (2000) The dispersal system of a butterfly: a test of source–sink theory suggests the intermediate-scale hypothesis. Am Nat 156:131–144

    CAS  PubMed  Google Scholar 

  • Bowers MD (1980) Unpalatability as a defense strategy of Euphydryas phaeton (Lepidoptera, Nymphalidae). Evolution 34:586–600

    Article  Google Scholar 

  • Bowers MD, Richardson LL (2013) Use of two oviposition plants in populations of Euphydryas phaeton, Drury (Nymphalidae). J Lepidopterists Soc 67:299–300

    Article  Google Scholar 

  • Bowers MD, Schmitt J (2013) Overcrowding leads to lethal oviposition mistakes in the Baltimore Checkerspot, Euphydryas phaeton, Drury (Nymphalidae). J Lepidopterists Soc 67:227–229

    Article  Google Scholar 

  • Bowers MD, Stamp NE, Collinge SK (1992) Early stage of host range expansion by a specialist herbivore, Euphydryas phaeton (Nymphalidae). Ecology 73:526–536

    Article  Google Scholar 

  • Brown LM, Crone EE (2016) Minimum area requirements for an at-risk butterfly based on movement and demography. Conserv Biol 30:103–112

    Article  PubMed  Google Scholar 

  • Carey JR (2001) Insect biodemography. Annu Rev Entomol 46:79–110

    Article  CAS  PubMed  Google Scholar 

  • Carpenter D, Cappuccino N (2005) Herbivory, time since introduction and the invasiveness of exotic plants. J Ecol 93:315–321

    Article  Google Scholar 

  • Caswell H (2001) Matrix population models, 2nd edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Cavers PB, Bassett IJ, Crompton CW (1980) The biology of Canadian weeds: 47. Plantago lanceolata L. Canadian J Plant Sci 60:1269–1282

    Article  Google Scholar 

  • Chew FS (1977) Coevolution of Pierid butterflies and their cruciferous foodplants. 2. Distribution of eggs on potential foodplants. Evolution 31:568–579

    Article  Google Scholar 

  • Cornell HV, Hawkins BA (1995) Survival patterns and mortality sources of herbivorous insects: some demographic trends. Am Nat 145:563–593

    Article  Google Scholar 

  • Cornell HV, Hawkins BA, Hochberg ME (1998) Towards an empirically-based theory of herbivore demography. Ecol Entomol 23:340–349

    Article  Google Scholar 

  • Courtney SP (1981) Coevolution of Pierid butterflies and their cruciferous foodplants. 3. Anthocharis cardamines (L) survival, development and oviposition on different hostplants. Oecologia 51:91–96

    Article  Google Scholar 

  • Emlen JM (1966) The role of time and energy in food preference. Am Nat 100:611–617

    Article  Google Scholar 

  • Fei M, Gols R, Harvey JA (2014) Seasonal phenology of interactions involving short-lived annual plants, a multivoltine herbivore and its endoparasitoid wasp. J Anim Ecol 83:234–244

    Article  PubMed  Google Scholar 

  • Fiske IJ, Chandler RB (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. J Stat Soft 43:1–23

    Article  Google Scholar 

  • Forister ML, Wilson JS (2013) The population ecology of novel plant–herbivore interactions. Oikos 122:657–666

    Article  Google Scholar 

  • Forister ML, Nice CC, Fordyce JA, Gompert Z (2009) Host range evolution is not driven by the optimization of larval performance: the case of Lycaeides melissa (Lepidoptera: Lycaenidae) and the colonization of alfalfa. Oecologia 160:551–561

    Article  PubMed  Google Scholar 

  • Frye J, Durkin P, Gibbs D, Gibbs R, Lustig M (2013) Conservation and management of the baltimore checkerspot (Euphydryas phaeton drury) in maryland: strategies for statewide monitoring and for wetland restoration, captive breeding and release in the piedmont region. In: Frye J (ed) Maryland department of natural resources, wildlife and heritage service, Natural heritage program, Annapolis, Maryland, USA

  • Fuchs A, Bowers MD (2004) Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age. J Chem Ecol 30:1723–1741

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Robledo C, Horvitz CC (2011) Experimental demography and the vital rates of generalist and specialist insect herbivores on native and novel host plants. J Anim Ecol 80:976–989

    Article  PubMed  Google Scholar 

  • Garcia-Robledo C, Horvitz CC (2012) Parent-offspring conflicts, “optimal bad motherhood” and the “mother knows best” principles in insect herbivores colonizing novel host plants. Ecol Evol 2:1446–1457

    Article  PubMed  PubMed Central  Google Scholar 

  • Gotelli N (2001) A primer of ecology, 3rd edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433

    Article  Google Scholar 

  • Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecol Lett 13:383–393

    Article  PubMed  Google Scholar 

  • Holt RD (1985) Population dynamics in two-patch environments: some anomalous consequences of an optimal habitat distribution. Theor Popul Biol 28:181–208

    Article  Google Scholar 

  • Janz N, Nylin S (2008) The oscillation hypothesis of host-plant range and speciation. In: Tilmon K (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 203–215

    Google Scholar 

  • Keeler MS, Chew FS (2008) Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156:559–568

    Article  PubMed  Google Scholar 

  • Kéry M, Schaub M (2012) Bayesian population analysis using WinBUGS: a hierarchical perspective. Academic Press, Elsevier, Waltham, MA, USA

    Google Scholar 

  • Kuussaari M, Van Nouhuys S, Hellmann JJ, Singer MC (2004) Larval biology of checkerspots. In: Ehrlich PR, Hanski I (eds) On the wings of checkerspots: a model system for population biology. Oxford University Press, New York, pp 138–160

    Google Scholar 

  • Lei GC, Hanski I (1997) Metapopulation structure of Cotesia melitaearum, a specialist parasitoid of the butterfly Melitaea cinxia. Oikos 78:91–100

    Article  Google Scholar 

  • Levins R, MacArthur R (1969) An hypothesis to explain the incidence of monophagy. Ecology 50:910–911

    Article  Google Scholar 

  • Mayhew PJ (2001) Herbivore host choice and optimal bad motherhood. Trends Ecol Evol 16:165–167

    Article  PubMed  Google Scholar 

  • Pearse IS, Altermatt F (2013) Predicting novel trophic interactions in a non-native world. Ecol Lett 16:1088–1094

    Article  PubMed  Google Scholar 

  • Pickens BA, Root KV (2008) Factors affecting host-plant quality and nectar use for the Karner blue butterfly: implications for oak savanna restoration. Nat Area J 28:210–217

    Article  Google Scholar 

  • Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661

    Article  Google Scholar 

  • Rodgers VL, Stinson KA (2008) Ready or not, garlic mustard is moving in: Alliaria petiolata as a member of eastern North American forests. Bioscience 58:426–436

    Article  Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939

    Article  Google Scholar 

  • Scheirs J, De Bruyn L, Verhagen R (2000) Optimization of adult performance determines host choice in a grass miner. P Roy Soc B-Biol Sci 267:2065–2069

    Article  CAS  Google Scholar 

  • Schlaepfer MA, Sax DF, Olden JD (2011) The potential conservation value of non-native species. Conserv Biol 25:428–437

    Article  PubMed  Google Scholar 

  • Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404

    Article  Google Scholar 

  • Severns PM, Warren A (2008) Selectively eliminating and conserving exotic plants to save an endangered butterfly from local extinction. Anim Conserv 11:476–483

    Article  Google Scholar 

  • Sih A, Christensen B (2001) Optimal diet theory: when does it work, and when and why does it fail? Anim Behav 61:379–390

    Article  Google Scholar 

  • Singer MC, McBride CS (2010) Multitrait, host-associated divergence among sets of butterfly populations: implications for reproductive isolation and ecological speciation. Evolution 64:921–933

    Article  PubMed  Google Scholar 

  • Singer MC, Thomas CD, Parmesan C (1993) Rapid human-induced evolution of insect host associations. Nature 366:681–683

    Article  Google Scholar 

  • Singer MC, Wee B, Hawkins S, Butcher M (2008) Rapid natural and anthropogenic diet evolution: three examples from checkerspot butterflies. In: Tilmon K (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. The University of California Press, Berkeley, pp 311–324

    Google Scholar 

  • Stamp NE (1979) New oviposition plant for Euphydryas phaeton (Nymphalidae). J Lepidopterists Soc 33:203–204

    Google Scholar 

  • Stamp NE (1981) Effect of group size on parasitism in a natural population of the Baltimore checkerspot, Euphydryas-Phaeton. Oecologia 49:201–206

    Article  Google Scholar 

  • Stamp NE (1982) Searching behavior of parasitoids for web-making caterpillars—a test of optimal searching theory. J Anim Ecol 51:387–395

    Article  Google Scholar 

  • Stamp NE (1984) Effect of defoliation by checkerspot caterpillars (Euphydryas phaeton) and sawfly larvae (Macrophya nigra and Tenthredo grandis) on their host plants (Chelone spp.). Oecologia 63:275–280

    Article  Google Scholar 

  • Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:354–371

    Article  Google Scholar 

  • Tepedino VJ, Bradley BA, Griswold TL (2008) Might flowers of invasive plants increase native bee carrying capacity? intimations from Capitol Reef National Park, Utah. Nat Area J 28:44–50

    Article  Google Scholar 

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Article  Google Scholar 

  • Van Nouhuys S, Hanski I (1999) Host diet affects extinctions and colonizations in a parasitoid metapopulation. J Anim Ecol 68:1248–1258

    Article  Google Scholar 

  • Wahlberg N (2001) The phylogenetics and biochemistry of host-plant specialization in melitaeine butterflies (Lepidoptera: Nymphalidae). Evolution 55:522–537

    Article  CAS  PubMed  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139

    Article  Google Scholar 

  • Wickman P-O, Karlsson B (1989) Abdomen size, body size and the reproductive effort of insects. Oikos 56:209–214

    Article  Google Scholar 

  • Williams EH (2012) Population loss and gain in the rare butterfly Euphydryas gillettii (Nymphalidae). J Lepidopterists Soc 66:147–155

    Article  Google Scholar 

  • Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711

    PubMed  Google Scholar 

  • Yoon S, Read Q (2016) Consequences of exotic host use: impacts on Lepidoptera and a test of the ecological trap hypothesis. Oecologia 181:985–996

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Conservation Commission of the town of Harvard, MA, for allowing us to use their land for our research. We also thank Aubrie James, Emma Sass, Natasha Tigreros, Norah Warchola, Ailene Ettinger, Lauren Redosh, Haley Coffman, Livia Baer-Bositis, Deane Bowers, Natalie Kerr, Dash Donnelly, Cheryl Schultz, Glenda Wardle, Michal Bodziewicz, and Rafal Zwolak for help with fieldwork. We are grateful to Richard Chandler for helpful advice regarding population models, and we are indebted to the Handling Editor and three anonymous reviewers for incredibly helpful comments and suggestions that greatly improved this manuscript. This work was supported by a National Science Foundation Award to LMB (DEB-1402287) and a Department of Defense SERDP Award to EEC (RC-2119), with additional support from Harvard Forest, Harvard University, and Tufts University.

Author contribution statement

EEC, GAB, and PMS conceived the original ideas and designed and carried out fieldwork conducted in 2012. LMB and EEC designed and carried out fieldwork conducted in 2013 and 2014. LMB and EEC collated and analyzed all of the data and wrote the manuscript.

Author information

Authors and Affiliations

  1. Odum School of Ecology, University of Georgia, 140 E. Green St, Athens, GA, USA

    Leone M. Brown

  2. Department of Biology, Tufts University, 163 Packard Ave, Medford, MA, USA

    Leone M. Brown & Elizabeth E. Crone

  3. Institute of Arctic Biology, University of Alaska Fairbanks, 902 N. Koyukuk Dr, Fairbanks, AK, USA

    Greg A. Breed

  4. Department of Botany and Plant Pathology, Oregon State University, 2082 Cordley Hall, Corvallis, OR, USA

    Paul M. Severns

Authors
  1. Leone M. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Greg A. Breed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul M. Severns
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth E. Crone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leone M. Brown.

Additional information

Communicated by Roland A. Brandl.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brown, L.M., Breed, G.A., Severns, P.M. et al. Losing a battle but winning the war: moving past preference–performance to understand native herbivore–novel host plant interactions. Oecologia 183, 441–453 (2017). https://doi.org/10.1007/s00442-016-3787-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-016-3787-y

Keywords

Search

Navigation