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Reversal of fortune: plant suppression and recovery after vole herbivory

  • Plant-Animal Interactions - Original Article
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Abstract

It is not clear how plant species preferred as forage by rodents persist in prairie vegetation. To test permanence of suppression of wet-mesic prairie vegetation by vole (Microtus pennsylvanicus) herbivory in synthetic experimental communities, access treatments were reversed after 9 years of vole exclusion or access. Between 1996 and 2004, rye grass Elymus virginicus (Poaceae) and tick-trefoil Desmodium canadense (Fabaceae) achieved mean cover of up to 30 and 25%, respectively, in plots where voles were excluded, but disappeared from plots where voles had access. To determine whether these species remained vulnerable to vole herbivory as established adults, and to determine whether the species could recover if vole herbivory were removed, access treatments were reversed at the end of the 2004 growing season and monitored through 2007. Repeated measures ANOVA demonstrated dramatic vole suppression of established E. virginicus, but not D. canadense, indicating continuing vulnerability of the grass but not of the adult legume. Release from vole herbivory resulted in re-growth of rye, but not tick-trefoil, which was apparently suppressed by established vegetation. Two additional common planted species did not respond to treatment reversal, nor did 11 much less common planted species that comprised a minor portion of the vegetation. Dominant perennial black-eyed Susan Rudbeckia subtomentosa (Asteraceae) did not change in plant numbers by year or treatment, but expanded or contracted in stems per plant and cover as E. virginicus was suppressed or released by vole herbivory or its absence. Results indicate that preferred food plants may persist through capacity to quickly recover during periods of relative vole scarcity, or reach a refuge in maturity.

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References

  • Batzli GO, Pitelka FA (1970) Influence of meadow mouse populations on California grassland. Ecology 51:1027–1039

    Article  Google Scholar 

  • Beckstead J, Parker IM (2003) Invasiveness of Amophila arenaria: release from soil-borne pathogens? Ecology 84:2824–2831

    Article  Google Scholar 

  • Beisner BE, Haydon DT, Cuddington K (2003) Alternative stable states in ecology. Front Ecol Environ 7:376–382

    Google Scholar 

  • Belsky AJ (1987) The effects of grazing: confounded the ecosystem, community, and organism scales. Am Nat 129:777–783

    Article  Google Scholar 

  • Belsky AJ (1992) Effects of grazing, competition, disturbance and fire on species composition and diversity in grassland communities. J Veg Sci 3:187–200

    Article  Google Scholar 

  • Bonsall MB, van der Meijden E, Crawley MJ (2003) Contrasting dynamics in the same plant–herbivore interactions. Proc Natl Acad Sci USA 100:14932–14936

    Article  PubMed  CAS  Google Scholar 

  • Brown JH, Heske EJ (1990) Control of a desert–grassland transition by a keystone rodent guild. Science 250:1705–1707

    Article  PubMed  Google Scholar 

  • Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744

    Article  PubMed  CAS  Google Scholar 

  • Clay K, Holah J, Rudgers JA (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc Natl Acad Sci USA 102:12465–12470

    Article  PubMed  CAS  Google Scholar 

  • Collins SL (1987) Interaction of disturbances in tallgrass prairie: a field experiment. Ecology 68:1243–1250

    Article  Google Scholar 

  • Del-Val E, Crawley MJ (2005) What limits herb biomass in grasslands: competition or herbivory? Oecologia 142:202–211

    Article  PubMed  Google Scholar 

  • Dublin HT, Sinclair ARE, McGlade J (1990) Elephants and fire as causes of multiple stable states in the Serengeti-Mara woodlands. J Anim Ecol 59:1147–1164

    Article  Google Scholar 

  • Edwards GR, Crawley MJ (1999) Rodent seed predation and seedling recruitment in mesic grassland. Oecologia 118:288–296

    Article  Google Scholar 

  • Galatowitsch SM, van der Valk AG (1996) The vegetation of restored and natural prairie wetlands. Ecol Appl 6:102–112

    Article  Google Scholar 

  • Glenn-Lewin DC, Johnson JL, Jurik T, Akey A, Loeschke M, Rosburg T (1990) Fire in Central North American grasslands: vegetative reproduction, seed germination, and seedling establishment. In: Collins SL, Wallace LL (eds) Fire in North American tall grass prairie. University of Oklahoma Press, Norman, pp 28–45

    Google Scholar 

  • Hambäck PA, Oksanen L, Ekerholm P, Lindgren Å, Oksanen T, Schneider M (2004) Predators indirectly protect tundra plants by reducing herbivore abundance. Oikos 106:85–92

    Article  Google Scholar 

  • Howe HF, Brown JS (1999) Effects of birds and rodents on synthetic tallgrass Communities. Ecology 80:1776–1781

    Google Scholar 

  • Howe HF, Brown JS (2000) Early consequences of rodent granivory on synthetic dicot communities. Ecol Appl 10:917–924

    Article  Google Scholar 

  • Howe HF, Brown JS (2001) The ghost of granivory past. Ecol Lett 4:371–378

    Article  Google Scholar 

  • Howe HF, Lane D (2004) Vole-driven succession in experimental wet prairie restorations. Ecol Appl 14:1295–1305

    Article  Google Scholar 

  • Howe HF, Brown JS, Zorn-Arnold B (2002) A rodent plague on prairie diversity. Ecol Lett 5:30–36

    Article  Google Scholar 

  • Howe HF, Zorn-Arnold B, Sullivan A, Brown JS (2006) Massive and distinctive effects of meadow voles on grassland vegetation. Ecology 87:3007–3013

    Article  PubMed  Google Scholar 

  • Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503

    Article  Google Scholar 

  • Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460

    Article  Google Scholar 

  • Jackson HHT (1961) The mammals of Wisconsin. University of Wisconsin Press, Madison

    Google Scholar 

  • Jordan WRIII, Gilpin ME, Aber JD (1987) Restoration ecology: ecological restoration as a technique for basic research. In: Jordan WRIII, Gilpin ME, Aber JD (eds) Restoration ecology: a synthetic approach to ecological research. Cambridge University Press, Cambridge, pp 3–22

    Google Scholar 

  • Keesing F (2000) Cryptic consumers and the ecology of an African savanna. Bioscience 50:205–215

    Article  Google Scholar 

  • Klemola T, Pettersen T, Stenseth NC (2003) Trophic interactions in population cycles of voles and lemmings: a model-based synthesis. Adv Ecol Res 33:75–160

    Article  Google Scholar 

  • Knapp AK, Blair JM, Briggs JM, Collins SL, Hartnett DC, Johnson LC, Towne EG (1999) The keystone role of bison in North American tallgrass prairie. Bioscience 49:39–50

    Article  Google Scholar 

  • Kurten B, Anderson E (1980) Pleistocene mammals of North America. Columbia University Press, New York

    Google Scholar 

  • Lawton JH (1999) Are there general laws in ecology? Oikos 84:177–192

    Article  Google Scholar 

  • Lin YK, Batzli G (2001) The influence of habitat quality on dispersal, demography, and population dynamics of voles. Ecol Monogr 71:245–275

    Google Scholar 

  • Manson RH, Ostfeld RS, Canham CD (2001) Long-term effects of rodent herbivores on tree invasion dynamics along forest–field edges. Ecology 82:3320–3329

    Google Scholar 

  • Marquis RJ, Batzli GO (1989) Influence of chemical factors on palatability of forage to voles. J Mammal 70:503–511

    Article  Google Scholar 

  • Massey FP, Ennos AR, Hartley SE (2007a) Grasses and the resource availability hypothesis: the importance of silica-based defences. J Ecol 95:414–424

    Article  CAS  Google Scholar 

  • Massey FP, Ennos AR, Hartley SE (2007b) Herbivore specific induction of silica-based plant defenses. Oecologia 152:677–683

    Article  PubMed  Google Scholar 

  • McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 55:259–294

    Article  Google Scholar 

  • Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265

    Article  Google Scholar 

  • Olofsson J, Moen J, Oksanen L (2002) Effects of herbivory on competition intensity in two arctic–alpine tundra communities with different productivity. Oikos 96:265–272

    Article  Google Scholar 

  • Olofsson J, Hulme PE, Oksanen L, Suominen O (2004) Importance of large and small mammalian herbivores for the plant community structure in the forest tundra ecotone. Oikos 106:324–334

    Article  Google Scholar 

  • Olofsson J, Hulme PE, Oksanen L, Suominen O (2005) Effects of mammalian herbivores on revegetation of disturbed areas in the forest–tundra ecotone in northern Fennoscandia. Landsc Ecol 20:351–359

    Article  Google Scholar 

  • Olofsson J, de Mazancourt C, Crawley MJ (2007) Contrasting effects of rabbit exclusion on nutrient availability and primary production in grasslands at different time scales. Oecologia 150:582–589

    Article  PubMed  Google Scholar 

  • Ostfeld RS, Manson RH, Canham CD (1997) Effects of rodents on survival of tree seeds and seedlings invading old fields. Ecology 78:1531–1542

    Article  Google Scholar 

  • Pacala SW, Crawley MJ (1992) Herbivores and plant diversity. Am Nat 140:243–260

    Article  PubMed  CAS  Google Scholar 

  • Prittinen K, Pusenius J, Tahvanainen J, Rousi M, Heinonen J, Roininen H (2006) Herbivory modifies the genetic structure of birch populations. Oikos 114:465–470

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53

    Article  PubMed  Google Scholar 

  • Taitt MJ, Krebs CJ (1985) Population dynamics and cycles. In: Tamarin RH (ed) Biology of New World Microtus. Special publication no. 8. American Society of Mammalogists. Allan Press, Lawrence, pp 567–620

    Google Scholar 

  • Zorn-Arnold B, Brown JS, Howe HF (2006) Obvious and cryptic vole suppression of a prairie legume in experimental restorations. Int J Plant Sci 167:961–968

    Article  Google Scholar 

Download references

Acknowledgments

I am grateful to K. Braunskill, L. Oksanen, R. Ostfeld, C. Seltzer, A. Sullivan, M. Valencia, and J. Zambrano for comments on the manuscript, to L. Hansen, N. Howe, D. Pacheco, Y. Wang, D. Zaya, B. Zorn-Arnold for help with field or lab work, and to A. Sullivan for help with the figure. This project was supported by NSF grant DEB 0129081. Procedures conformed to US laws and permit regulations.

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Correspondence to Henry F. Howe.

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Communicated by Scott Collins.

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Howe, H.F. Reversal of fortune: plant suppression and recovery after vole herbivory. Oecologia 157, 279–286 (2008). https://doi.org/10.1007/s00442-008-1069-z

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