SpringerLink
Log in

Exotic vertebrate and invertebrate herbivores differ in their impacts on native and exotic plants: a meta-analysis

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Herbivores modify various ecological processes including interactions between native and exotic plants that may affect invasion success by the exotic plants. It is unknown whether different types of exotic herbivores have similar effects on native and exotic plants. Using two distinct data sets, we ran meta-analyses to compare exotic vertebrate and invertebrate herbivore preferences for, and effects on performance and population sizes of native and exotic plants. We found that exotic vertebrate herbivores have positive effects on exotic plant performance and population sizes, and no significant effects on native plants. Exotic invertebrates have significant negative effects on performance and population sizes of both exotic and native plants. Vertebrates prefer to feed on native plants relative to exotic plants, while invertebrates prefer the exotic plants to native plants. Thus the exotic vertebrate herbivores may aid invasiveness of exotic plants, in accordance with the invasional meltdown hypothesis, while exotic invertebrate herbivores probably have no net effect on invasion process of the exotic plants. Invertebrate herbivore preferences for exotic plants support the biotic resistance hypothesis, as the native plants probably resist the invertebrate herbivory. We also tested an evolutionary logic that posits that herbivores with similar evolutionary history as plants will affect the plants less negatively than plants with which they have not co-evolved. Our results indicate that there is no consistent pattern in effects of exotic vertebrate and invertebrate herbivores on exotic plants with or without which they have co-evolved.

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
EUR 32.99 /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 includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adler PB, Raff DA, Lauenroth WK (2001) The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128:465–479

    Article  Google Scholar 

  • Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecology Letters 6:712–715

    Google Scholar 

  • Baraza E, Zamora R, Hódar JA, Gómez JM (2007) Plant-herbivore interaction. Beyond a binary vision. In: Pugnaire FI, Valladares F (eds) Hand book of functional plant ecology, 2nd edn. CRC Press, Boca Ratón, pp 678–709

    Google Scholar 

  • Bergelson J (1990) Spatial patterning in plants—opposing effects of herbivory and competition. J Ecol 78:937–948

    Article  Google Scholar 

  • Best RJ, Arcese P (2009) Exotic herbivores directly facilitate the exotic grasses they graze:mechanisms for an unexpected positive feedback between invaders. Oecologia 159(1):139–150

    Google Scholar 

  • Bezemer TM, Jones TH (1998) Plant-insect herbivore interactions in elevated atmospheric CO2 quantitative analysis and guild effects. Oikos 82:212–222

    Article  Google Scholar 

  • Bisigato AJ, Bertiller MB, Ares JO, Pazos GE (2005) Effect of grazing on plant patterns in arid ecosystems of Patagonian Monte. Ecography 28:561–572

    Article  Google Scholar 

  • Bock CE, Bock JH, Kennedy L, Jones ZF (2007) Spread of non-native grasses into grazed versus ungrazed desert grasslands. J Arid Environ 71:229–235

    Article  Google Scholar 

  • Branson D, Sword G (2008) Grasshopper herbivory affects native plant diversity and abundance in grassland dominated by the exotic grass Agropyron cristatum. Restor Ecol 17:89–96

    Article  Google Scholar 

  • Campbell JE, Gibson DJ (2001) The effect of seeds of exotic species transported via horse dung on vegetation along trail corridors. Plant Ecol 157(1):23–25

    Article  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success affected by enemy release hypothesis? Ecol Lett 7:721–731

    Article  Google Scholar 

  • Crawley MJ (1989) The relative importance of vertebrate and invertebrate herbivores in plant population dynamics. In: Bernays EA (ed) Insect-plant interactions, vol 1. CRC press, Boca Raton, pp 45–71

    Google Scholar 

  • Cushman JH, Tierney TA, Hinds JM (2004) Variable effects of feral pig disturbances on native and exotic plants in a California grassland. Ecol Appl 14:1746–1756

    Article  Google Scholar 

  • Donlan CJ, Tershy BR, Croll DA (2002) Islands and exotic herbivores: conservation action as ecosystem experimentation. J Appl Ecol 39:235–246

    Article  Google Scholar 

  • Egan J, Irwin R (2008) Evaluation of the field impact of an adventitious herbivore on an invasive plant, yellow toadflax, in Colorado, USA. Plant Ecol 199:99–114

    Google Scholar 

  • Fischer SF, Poschlod P, Beinlich B (1996) Experimental studies on the dispersal of plants and animals on sheep in calcareous grasslands. J Appl Ecol 33:1206–1222

    Article  Google Scholar 

  • Focardi S, Tinelli A (2005) Herbivory in a Mediterranean forest: browsing impact and plant compensation. Acta Oecol Int J Ecol 28:239–247

    Article  Google Scholar 

  • Gill RMA (1992) A review of damage by mammals in north temperate forests.3. Impacts on trees and forests. Forestry 65:363–388

    Article  Google Scholar 

  • Gordon IJ (1989) Vegetation community selection by ungulates on the Isle of Rhum.III. Determinants of vegetation community selection. J Appl Ecol 26:65–79

    Article  Google Scholar 

  • Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149

    Article  Google Scholar 

  • Hanley ME, Sykes RJ (2009) Impact of seedling herbivory on plant competition and implications for species co-existence. Ann Bot. doi: 10.1093/aob/mcp081

  • Hanley ME, Fenner M, Edwards PJ (1996) The effect of mollusk grazing on seedling recruitment in artificially created grassland gaps. Oecologia 106:240–246

    Article  Google Scholar 

  • Hendrix SD (1990) Herbivory and its impact on plant reproduction. In: Doust JL, Doust LL (eds) Plant reproduction ecology: patterns and strategies, pp 246–259

  • Holmgren M (2002) Exotic herbivores as drivers of plant invasion and switch to ecosystem alternative states. Biol Invasions 4:25–33

    Article  Google Scholar 

  • Holmgren M, Avilés R, Sierralta L, Segura AM, Fuentes ER (2000) Why have European herbs so successfully invaded the Chilean matorral? Effects of herbivory, soil nutrients, and fire. J Arid Environ 44:197–211

    Article  Google Scholar 

  • Hulme PE (1994) Seedling herbivory in grassland: relative impact of vertebrate and invertebrate herbivores. J Ecol 82:873–880

    Article  Google Scholar 

  • Hulme PE (1996a) Herbivores and the performance of grassland plants: a comparison of arthropod, mollusk and rodent herbivory. J Ecol 84:43–51

    Article  Google Scholar 

  • Hulme PE (1996b) Herbivory, plant regeneration, and species coexistence. J Ecol 84:609–615

    Article  Google Scholar 

  • Janz N, Nylin S (1998) Butterflies and plants: a phylogenetic study. Evolution 52(2):486-502

    Google Scholar 

  • Janzen D (1984) Dispersal of small seeds by big herbivores-foliage is the fruit. Am Nat 123:338–353

    Article  Google Scholar 

  • Jasmin JN, Rochefort L, Gauthier G (2008) Goose grazing influences the fine-scale structure of a bryophyte community in arctic wetlands. Polar Biol 31:1043–1049

    Article  Google Scholar 

  • Joe SM, Daehler CC (2008) Invasive slugs as under-appreciated obstacles to rare plant restoration: evidence from the Hawaiian Islands. Biol Invasions 10:245–255

    Article  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Keeley JE, Lubin D, Fotheringham CJ (2003) Fire and grazing impacts on plant diversity and alien plant invasions in the southern Sierra Nevada. Ecol Appl 13(5):1355–1374

    Article  Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

    Article  Google Scholar 

  • Loeser MRR, Sisk TD, Crews TE (2007) Impact of grazing intensity during drought in an Arizona grassland. Conserv Biol 21(1):87–97

    Article  PubMed  Google Scholar 

  • Louda SM, Kendall D, Connor J, Simberloff D (1997) Ecological effects of an insect introduced for the biological control of weeds. Science 277:1088–1090

    Article  CAS  Google Scholar 

  • Louda SM, Arnett AE, Rand TA, Russell FL (2003) Invasiveness of some biological control insects and adequacy of their ecological risk assessment and regulation. Conserv Biol 17:73–82

    Article  Google Scholar 

  • Loydi A, Zalba SM (2008) Feral horses dung piles as potential invasion windows for alien plant species in natural grasslands. Plant Ecol 201:471–480

    Article  Google Scholar 

  • Malo JE, Suarez F (1995) Herbivorous mammals as seed dispersers in a Mediterranean Dehesa. Oecologia 104:246–255

    Article  Google Scholar 

  • Malo JE, Suarez F (1997) Dispersal mechanism and transcontinental naturalization proneness among Mediterranean herbaceous species. J Biogeogr 24:391–394

    Article  Google Scholar 

  • Manrique R, Gutiérrez JR, Holmgren M, Squeo FA (2007) Reduced herbivory during simulated ENSO rainy events increases native herbaceous plants in semiarid Chile. Plant Ecol 191:21–31

    Article  Google Scholar 

  • Manzano P, Malo JE (2006) Extreme long-distance seed dispersal via sheep. Front Ecol Environ 4:244–248

    Article  Google Scholar 

  • Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B 273:2575–2584

    Article  PubMed  Google Scholar 

  • Maron JL, Vilá M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • Mouissie M (2004) Seed dispersal by large herbivores: implications for the restoration of plant biodiversity. Ph.D. dissertation, Groningen University, The Netherlands

  • Myers JA, Vellend M, Gardescu S, Marks PL (2004) Seed dispersal by white-tailed deer: implications for long-distance dispersal, invasion, and migration of plants in eastern North America. Oecologia 139:35–44

    Article  PubMed  Google Scholar 

  • Nuñez MA, Relva MA, Simberloff D (2008) Enemy release or invasional meltdown? Deer preference for exotic and native trees on Isla Victoria, Argentina. Austral Ecol 33:317–323

    Article  Google Scholar 

  • Pakeman RJ (2001) Plant migration rates and seed dispersal mechanisms. J Biogeogr 28:795–800

    Article  Google Scholar 

  • Pakeman RJ, Digneffe G, Small JL (2002) Ecological correlates of endozoochory by herbivores. Funct Ecol 16:296–304

    Article  Google Scholar 

  • Palmisano S, Fox LR (1997) Effects of mammal and insect herbivory on population dynamics of a native California thistle, Cirsium occidentale. Oecologia 111:413–421

    Article  Google Scholar 

  • Parker JD, Deron E, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg MS, Dean CA, Gurevitch J (2000) Meta win-statistical software for meta-analysis. Version 2.0. Sinauer Associates Inc, Massachusetts

    Google Scholar 

  • Rosenthal R (1979) The ‘file drawer’ problem and tolerance for null results. Psychol Bull 86:638–641

    Article  Google Scholar 

  • Rosenthal JP, Dirzo R (1997) Effects of life history, domestication and agronomic selection on plant defence against insects: evidence from maizes and wild relatives. Evol Ecol 11:337–355

    Article  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University Press, Oxford, p 421

    Google Scholar 

  • Sessions LA, Kelly D (2001) Heterogeneity in vertebrate and invertebrate herbivory and its consequences for New Zealand mistletoes. Austral Ecol 26:571–581

    Article  Google Scholar 

  • Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919

    Article  PubMed  Google Scholar 

  • Stohlgren TJ, Schell LD, Vanden Heuvel B (1999) How grazing and soil quality affect native and exotic plant diversity in rocky mountain grasslands. Ecol Appl 9:45–64

    Article  Google Scholar 

  • Strauss SY (1991) Direct, indirect, and cumulative effects of three native herbivores on a shared host plant. Ecology 72:543–558

    Article  Google Scholar 

  • Strauss SY, Stanton ML, Emery NC, Bradley CR, Dittrich-Reed DR, Ervin OA, Gray LN, Hamilton AM, Harper SD, Law KN, Pham VQ, Putnam ME, Roth TM, Wells LM, Yoshizuka EM (2009) Cryptic predation by invertebrate nocturnal generalists may underlie survival, performance and fine-scale distribution of native and exotic plants. Ecology 90(2):419–429

    Article  PubMed  Google Scholar 

  • Tierney TA, Cushman JH (2006) Temporal changes in native and exotic vegetation and soil characteristics following disturbances by feral pigs in a California grassland. Biol Invasions 8:1073–1089

    Article  Google Scholar 

  • Vázquez DP (2002) Multiple effects of introduced mammalian herbivores in a temperate forest. Biol Invasions 4:175–191

    Article  Google Scholar 

  • Veen GF, Blair JM, Smith MD, Collins SL (2008) Influence of grazing and fire frequency on small-scale plant community structure and resource variability in native tallgrass prairie. Oikos 117:859–866

    Article  Google Scholar 

  • Vellend M, Myers JA, Gardescu S, Marks PL (2003) Dispersal of Trillium seeds by deer: Implications for long-distance migration of forest herbs. Ecology 84:1067–1072

    Article  Google Scholar 

  • Waldbauer G (2003) What good are bugs? Insects in the web of life. Harvard University press, Cambridge, p 366

    Google Scholar 

  • Yates CJ, Norton DA, Hobbs RJ (2000) Grazing effects on plant cover, soil and microclimate in fragmented woodlands in south-western Australia: implications for restoration. Austral Ecol 25:36–47

    Google Scholar 

Download references

Acknowledgments

We thank Martín A. Nuñez for inviting us to write this review and Kimberly J. Komatsu for providing unpublished data. Lyn A. Gettys provided published data that were otherwise inaccessible to us. A grant from the foundation Banco Bilbao Vizcaya Argentaria (BBVA-BIOCON06/064) partly supported this study.

Author information

Authors and Affiliations

  1. Dpto de Ecología, Universidad de Granada, 18071, Granada, Spain

    Ayub M. O. Oduor & José M. Gómez

  2. Section of Evolution and Ecology, University of California Davis, One Shields Avenue, Davis, CA, 95616, USA

    Sharon Y. Strauss

Authors
  1. Ayub M. O. Oduor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José M. Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sharon Y. Strauss
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ayub M. O. Oduor.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 87 kb)

(DOC 238 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oduor, A.M.O., Gómez, J.M. & Strauss, S.Y. Exotic vertebrate and invertebrate herbivores differ in their impacts on native and exotic plants: a meta-analysis. Biol Invasions 12, 407–419 (2010). https://doi.org/10.1007/s10530-009-9622-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-009-9622-1

Keywords

Search

Navigation