, Volume 166, Issue 3, pp 649–657 | Cite as

Invasive plant species alters consumer behavior by providing refuge from predation

  • Humberto P. DutraEmail author
  • Kirk Barnett
  • Jason R. Reinhardt
  • Robert J. Marquis
  • John L. Orrock
Plant-Animal interactions - Original Paper


Understanding the effects of invasive plants on native consumers is important because consumer-mediated indirect effects have the potential to alter the dynamics of coexistence in native communities. Invasive plants may promote changes in consumer pressure due to changes in protective cover (i.e., the architectural complexity of the invaded habitat) and in food availability (i.e., subsidies of fruits and seeds). No experimental studies have evaluated the relative interplay of these two effects. In a factorial experiment, we manipulated cover and food provided by the invasive shrub Amur honeysuckle (Lonicera maackii) to evaluate whether this plant alters the foraging activity of native mammals. Using tracking plates to quantify mammalian foraging activity, we found that removal of honeysuckle cover, rather than changes in the fruit resources it provides, reduced the activity of important seed consumers, mice in the genus Peromyscus. Two mesopredators, Procyon lotor and Didelphis virginiana, were also affected. Moreover, we found rodents used L. maackii for cover only on cloudless nights, indicating that the effect of honeysuckle was weather-dependent. Our work provides experimental evidence that this invasive plant species changes habitat characteristics, and in so doing alters the behavior of small- and medium-sized mammals. Changes in seed predator behavior may lead to cascading effects on the seeds that mice consume.


Loniceramaackii Foraging activity Indirect effects Peromyscusleucopus Predation risk 



We thank numerous field assistants from various school districts in the St. Louis area that volunteered as field assistants; the Marquis Lab for reading early drafts of this manuscript; Missouri Department of Conservation and John Vogel from Busch Wildlife Conservation Area for helping in the logistics and allowing us to work in their Park. This project was funded by a dissertation improvement grant (NSF # 0710341) and grants from the Webster Groves Nature Study Society and the Whitney R. Harris World Ecology Center.


  1. Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conserv Biol 17:267–272. doi: 10.1046/j.1523-1739.2003.01260.x CrossRefGoogle Scholar
  2. Allan BF, Dutra HP, Goessling LS, Barnett K, Chase JM, Marquis RJ, Pang G, Storch GA, Thach RE, Orrock JL (2010) Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proc Natl Acad Sci USA 107:18523–18527. doi: 10.1073/pnas.1008362107 PubMedCrossRefGoogle Scholar
  3. Anderson CS, Cady AB, Meikle B (2003) Effects of vegetation structure and edge habitat on the density and distribution of white-footed mice (Peromyscus leucopus) in small and large forest patches. Can J Zool 81:897–904. doi: 10.1139/z03-074 CrossRefGoogle Scholar
  4. Anderson CS, Meikle DB, Cady AB, Schaefer RL (2006) Annual variation in habitat use by White-footed Mice, Peromyscus leucopus: the effects of forest patch size, edge and surrounding vegetation type. Can Field Nat 120:192–198. doi: 10.1139/z03-074 Google Scholar
  5. Azevedo FCC, Lester V, Gorsuch W, Lariviere S, Wirsing AJ, Murray DL (2006) Dietary breadth and overlap among five sympatric prairie carnivores. J Zool 269:127–135. doi: 10.1111/j.1469-7998.2006.00075.x CrossRefGoogle Scholar
  6. Bartuszevige AM, Hughes MR, Bailer AJ, Gorchov DL (2006) Weather-related patterns of fruit abscission mask patterns of frugivory. Can J Bot 84:869–875. doi: 10.1007/s10530-005-3634-2 CrossRefGoogle Scholar
  7. Beasley JC, Devault TL, Retamosa MI, Rhodes OE (2007) A Hierarchical analysis of habitat selection by raccoons in northern Indiana. J Wildl Manag 71:125–1133. doi: 10.2193/2006-228 Google Scholar
  8. Borer ET, Hosseini PR, Seabloom EW, Dobson AP (2007) Pathogen-induced reversal of native dominance in a grassland community. Proc Natl Acad Sci USA 104:5473–5478PubMedCrossRefGoogle Scholar
  9. Bowman GB, Harris LD (1980) Effect of spatial heterogeneity on ground-nest depredation. J Wildl Manag 4:806–813. doi: 10.2307/3808308 Google Scholar
  10. Bradley JE, Marzluff JM (2003) Rodents as nest predators: influences on predatory behavior and consequences to nesting birds. Auk 1120:1180–1187. doi: 10.1642/0004-8038(2003)120[1180:RANPIO]2.0.CO;2 CrossRefGoogle Scholar
  11. Brown JS, Morgan RA, Dow BD (1992) Patch use under predation risk: II a test with fox squirrels, Sciurus niger. Ann Zool Fenn 29:37–47Google Scholar
  12. Chamberlain MJ, Conner LM, Leopold BD, Hodges KM (2003) Space use and multi-scale habitat selection of adult raccoons in central Mississippi. J Wildl Manag 67:334–340. doi: 10.2307/3802775 CrossRefGoogle Scholar
  13. Collier M, Vankat J, Hughes M (2002) Diminished plant richness and abundance below Lonicera maackii, an invasive shrub. Am Mid Nat 147:60–71CrossRefGoogle Scholar
  14. Connors MJ, Schauber EM, Forbes A, Jones CC, Goodwin BJ, Ostfeld RS (2005) Use of track plates to quantify predation risk at small spatial scales. J Mammal 86:991–996. doi: 10.1644/1545-1542(2005)86[991:UOTPTQ]2.0.CO;2 CrossRefGoogle Scholar
  15. Edalgo JA, McChesney EM, Love JP, Anderson JT (2009) Microhabitat use by white-footed mice Peromyscus leucopus in forested and old-field. Curr Zool 55:111–122Google Scholar
  16. Elbrock M (2003) Mammal tracks, sign: a guide to North American species. Stackpole, MechanisburgGoogle Scholar
  17. Elkinton JS, Healy WM, Buonaccorsi JP, Hazzard AM, Smith HR, Liebhold AM (1996) Interactions among gypsy moths, white-footed mice, and acorns. Ecology 77:2332–2342. doi: 10.2307/2265735 CrossRefGoogle Scholar
  18. Forseth IN Jr, Innis AF (2004) Kudzu (Pueraria montana): history, physiology, and ecology combine to make a major ecosystem threat. Crit Rev Plant Sci 23:401–413. doi: 10.1080/07352680490505150 CrossRefGoogle Scholar
  19. Gehrt S, Fritzell E (1998) Resource distribution, female home range dispersion and male spatial interactions: group structure in a solitary carnivore. Anim Behav 55:1211–1227PubMedCrossRefGoogle Scholar
  20. Gorchov DL, Trisel DE (2003) Competitive effects of the invasive shrub, Lonicera maackii (rupr.) Herder (Caprifoliaceae), on the growth and survival of the native tree seedlings. Plant Ecol 166:13–24. doi: 10.1023/A:1023208215796 CrossRefGoogle Scholar
  21. Gosper CR, Whelan RJ, French K (2006) The effect of invasive plant management on the rate of removal of vertebrate-dispersed fruits. Plant Ecol 184:351–363. doi: 10.1007/s11258-005-9078-z CrossRefGoogle Scholar
  22. Gould AMA, Gorchov DL (2000) Effects of the exotic invasive shrub Lonicera maackii on the survival and fecundity of three species of native annuals. Am Midl Nat 144:36–50. doi: 10.1674/0003-0031(2000)144[0036:EOTEIS]2.0.CO;2 CrossRefGoogle Scholar
  23. Gu L, Hanson PJ, Mac Posy W, Kaiser DP, Yang B, Nemani R, Pallardy SG, Meyers T (2008) The 2007 eastern US spring freezes: increased cold damage in a warming world? Bioscience 5:253–262. doi: 10.1641/B580311 CrossRefGoogle Scholar
  24. Hartman K, McCarthy B (2008) Changes in forest structure and species composition following invasion by a non-indigenous shrub, Amur honeysuckle (Lonicera maackii). J Torr Bot Soc 135:245–259CrossRefGoogle Scholar
  25. Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conserv Biol 11:1117–1124. doi: 10.1046/j.1523-1739.1997.96001.x CrossRefGoogle Scholar
  26. Hutchinson TF, Vankat JL (1999) Landscape structure and spread of the exotic shrub Lonicera maackii (Amur honeysuckle) in southwestern Ohio forests. Am Midl Nat 139:383–390. doi: 10.1674/0003-0031(1998)139[0383:LSASOT]2.0.CO;2 CrossRefGoogle Scholar
  27. Ingold JL, Craycraft MJ (1983) Avian frugivory on honeysuckle (Lonicera) in Southwestern Ohio in fall. Ohio J Sci 83:256–258Google Scholar
  28. Jones CG, Ostfeld RS, Richard MP, Schauber EM, Wolff JO (1998) Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279:1023–1026. doi: 10.1126/science.279.5353.1023 PubMedCrossRefGoogle Scholar
  29. Korpimäki E, Koivunen V, Hakkarainen H (1996) Microhabitat use and behavior of voles under weasel and raptor predation risk: predator facilitation? Behav Ecol 7:30–34. doi: 10.1093/beheco/7.1.30 CrossRefGoogle Scholar
  30. Kotler BP (1997) Patch use by gerbils in a risky environment: manipulating food and safety to test four models. Oikos 78:274–282. doi: 10.2307/3546294 CrossRefGoogle Scholar
  31. Kotler BP, Brown JS, Hasson O (1991) Factors affecting gerbil foraging behavior and rates of owl predation. Ecology 72:2249–2260. doi: 10.2307/1941575 CrossRefGoogle Scholar
  32. Levine JM, Vilá M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B 270:775–781. doi: 10.1098/rspb.2003.2327 CrossRefGoogle Scholar
  33. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. doi: 10.1139/z90-092 CrossRefGoogle Scholar
  34. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute, Cary. doi: 10.1080/10543400601001600 Google Scholar
  35. Luken JO, Goessling N (1995) Seedling distribution and potential persistence of the exotic shrub Lonicera maackii in fragmented forests. Am Midl Nat 133:124–130. doi: 10.2307/2426353 CrossRefGoogle Scholar
  36. Luken JO, Thieret JW (1996) Amur honeysuckle its fall from grace. Bioscience 46:18–24. doi: 10.2307/1312651 CrossRefGoogle Scholar
  37. Luken JO, Kuddes LM, Tholemeier TC (1997) Response of understory species to gap formation and soil disturbance in Lonicera maackii thickets. Restor Ecol 5:229–235. doi: 10.1046/j.1526-100X1997.09727.x CrossRefGoogle Scholar
  38. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. doi: 10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2 CrossRefGoogle Scholar
  39. Manson RH, Ostfeld RS, Canham CD (1998) The effects of tree seed and seedling density on predation rates by rodents in old fields. Ecoscience 5:183–190Google Scholar
  40. Manson RH, Ostfeld RS, Canham CD (1999) Responses of a small mammal community to heterogeneity along forest—old-field edges. Landscape Ecol 14:355–367. doi: 10.1023/A:1008093823391 CrossRefGoogle Scholar
  41. Mattos KJ, Orrock JL (2010) Behavioral consequences of plant invasion: an invasive plant alters rodent anti-predator behavior. Behav Ecol 21:556–561. doi: 10.1093/beheco/arq020 CrossRefGoogle Scholar
  42. McCusker C, Ward M, Brawn J (2010) Seasonal responses of avian communities to invasive bush honeysuckles (Lonicera spp). Biol Invasion 12:2459–2470. doi: 10.1007/s10530-009-9655-5 CrossRefGoogle Scholar
  43. Meiners SJ (2007) Apparent competition: an impact of exotic shrub invasion on tree regeneration. Biol Invasion 9:849–855. doi: 10.1007/s10530-006-9086-5 CrossRefGoogle Scholar
  44. Miller K, Gorchov D (2004) The invasive shrub, Lonicera maackii, reduces growth and fecundity of perennial forest herbs. Oecologia 139:359–375. doi: 10.1007/s00442-004-1518-2 PubMedCrossRefGoogle Scholar
  45. Mohr K, Solveig VP, Jeppesen LL, Bildose M, Leir H (2003) Foraging of multimammate, Mastomys natalensis, under different predation pressure: cover, patch-dependent decisions and density-dependent GUDs. Oikos 100:459–468. doi: 10.1034/j.1600-0706.2003.11763.x CrossRefGoogle Scholar
  46. Noonburg EG, Byers JE (2005) More harm than good: when invader vulnerability to predators enhances impact on native species. Ecology 86:2555–2560. doi: 10.1890/05-0143 CrossRefGoogle Scholar
  47. Orrock JL, Danielson BJ (2004) Rodents balancing a variety of risks: invasive fire ants and indirect and direct indicators of predation risk. Oecologia 140:1–6. doi: 10.1007/s00442-004-1613-4 CrossRefGoogle Scholar
  48. Orrock JL, Danielson BJ (2009) Temperature and cloud cover, but not predator urine, affect winter foraging of mice. Ethology 115:641–648. doi: 10.1111/j.1439-0310.2009.01654.x CrossRefGoogle Scholar
  49. Orrock JL, Danielson BJ, Brinkerhoff RJ (2004) Rodent foraging is affected by indirect, but not by direct, cues of predation risk. Behav Ecol 15:433–437. doi: 10.1093/beheco/arh031 CrossRefGoogle Scholar
  50. Orrock JL, Holt RD, Baskett ML (2010a) Refuge-mediated apparent competition in plant–consumer interactions. Ecol Lett 13:11–20. doi: 10.1111/j.1461-0248.2009.01412.x PubMedCrossRefGoogle Scholar
  51. Orrock JL, Baskett ML, Holt RD (2010b) Spatial interplay of plant competition and consumer foraging mediate plant coexistence and drive the invasion ratchet. Proc R Soc Lond B 277:3307–3315. doi: 10.1098/rspb.2010.0738 CrossRefGoogle Scholar
  52. Ostfeld RS, Manson RH, Canham CD (1997) Effects of rodents on survival of tree seeds and seedlings invading old fields. Ecology 78:1531–1542Google Scholar
  53. Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791. doi: 10.1525/bio.2009.59.9.9 CrossRefGoogle Scholar
  54. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  55. Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93. doi: 10.1017/S0006323199005435 PubMedCrossRefGoogle Scholar
  56. Rodewald AD, Shustack DP, Hitchcoc LE (2010) Exotic shrubs as ephemeral ecological traps for nesting birds. Biol Invasion 12:33–39. doi: 10.1007/s10530-009-9426-3 CrossRefGoogle Scholar
  57. SAS Institute (2000) SAS User’s Guide, Version 9.1.3. SAS Institute, Cary, NCGoogle Scholar
  58. Schmidt KA, Whelan CJ (1999) Effects of exotic Lonicera and Rhamnus on songbird nest predation. Conserv Biol 13:1502–1506. doi: 10.1046/j.1523-1739.1999.99050.x CrossRefGoogle Scholar
  59. Sheley RL, Jacobs JS, Carpinelli MF (1998) Distribution, biology, and management of Diffuse Knapweed (Centaurea diffusa) and Spotted Knapweed (Centaurea maculosa). Weed Technol 12:353–362Google Scholar
  60. Staller EL, Palmer WE, Carroll JP, Thornton RP, Sisson DC (2005) Identifying predators at northern bobwhite nests. J Wildlife Manag 69:124–132. doi: 10.2193/0022-541X(2005)069<0124%3AIPANBN>2.0.CO%3B2 CrossRefGoogle Scholar
  61. Stansbury CD, Vivian-Smith G (2003) Interactions between frugivorous birds and weeds in Queensland as determined from a survey of birders. Plant Prot Quart 18:157–165Google Scholar
  62. Vander Wall SB (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117. doi: 10.1007/BF02857850 CrossRefGoogle Scholar
  63. Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464. doi: 10.1007/s00265-006-0172-6 CrossRefGoogle Scholar
  64. Wiewel AS, Clark WA, Sovada MA (2007) Assessing small mammal abundance with track-tube indices and mark-recapture population estimates. J Mammal 88:250–260. doi: 10.1644/06-MAMM-A-098R1.1 CrossRefGoogle Scholar
  65. Williams CE, Ralley JJ, Taylor DH (1992) Consumption of seeds of the invasive Amur honeysuckle, Lonicera maackii (Rupr.) Maxim., by small mammals. Nat Area J 12:86–89Google Scholar
  66. Williams SE, Ward JS, Worthley TE, Stafford KC (2009) Managing japanese barberry (Ranunculales: Berberidaceae) infestations reduces blacklegged tick (Acari: ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environ Entomol 38:977–984. doi: 10.1603/022.038.0404 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Humberto P. Dutra
    • 1
    Email author
  • Kirk Barnett
    • 2
  • Jason R. Reinhardt
    • 2
  • Robert J. Marquis
    • 2
  • John L. Orrock
    • 3
  1. 1.Department of Natural SciencesLife UniversityMariettaUSA
  2. 2.Department of BiologyUniversity of Missouri-St. LouisSt. LouisUSA
  3. 3.Department of ZoologyUniversity of WisconsinMadisonUSA

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