Skip to main content

Advertisement

SpringerLink
Log in

Native granivores reduce the establishment of native grasses but not invasive Bromus tectorum

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

Abstract

Seed predation can structure plant communities by imposing strong population controls on some species but not others. In this context, studies from various ecosystems report that native granivores selectively forage for seeds from native species over seeds from exotic invaders, which could disproportionately favor the establishment of invaders and facilitate their dominance in communities. However, few studies have connected selective foraging for native seeds to differential patterns of establishment among native and invasive species. Thus, the extent to which preferential foraging for native seeds favors the establishment of invasive plants is unclear. Here, we used experimental seed additions and exclosure treatments at five field sites distributed across ≈ 80,000 km2 of the Great Basin Desert, USA to compare the effects of rodent foraging on the establishment of less-preferred cheatgrass (Bromus tectorum—an annual species native to Eurasia that is exotic and highly invasive across the Great Basin) and four species of more-preferred native grasses that commonly co-occur with cheatgrass. Rodent foraging reduced the establishment of each native species by at least 80% but had no effect on the establishment of cheatgrass, and this finding was consistent across study sites. Our results suggest that selective foraging for native species may favor the establishment of cheatgrass over native grasses, potentially exacerbating one of the most extensive plant invasions in North America.

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

Similar content being viewed by others

References

  • Allen PS, Benech-Arnold RL, Batlla D, Bradford KJ (2007) Modeling of seed dormancy. In: Bradford KJ, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell Publishing, Oxford, pp 72–112

    Chapter  Google Scholar 

  • Andersen AN (1989) How important is seed predation to recruitment in stable populations of long-lived perennials? Oecologia 81:310–315

    Article  PubMed  Google Scholar 

  • Balch JK, Bradley BA, D’Antonio CM, Gomez-Dans J (2013) Introduced annual grass increases regional fire activity across the arid western USA (1980–2009). Glob Change Biol 19:173–183

    Article  Google Scholar 

  • Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20

    Article  Google Scholar 

  • Blaney CS, Kotanen PM (2001) Post-dispersal losses to seed predators: an experimental comparison of native and exotic old field plants. Can J Bot 79:284–292

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  CAS  PubMed  Google Scholar 

  • Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438

    Article  PubMed  PubMed Central  Google Scholar 

  • Clair St. SB, O’Connor R, Gill R, McMillan B (2016) Biotic resistance and disturbance: rodent consumers regulate post-fire plant invasions and increase plant community diversity. Ecology 97:1700–1711

    Article  Google Scholar 

  • Ceradini JP, Chalfoun AD (2017) Species’ traits help predict small mammal responses to habitat homogenization by an invasive grass. Ecol Appl 27:1451–1465

    Article  PubMed  Google Scholar 

  • Charnov EL (1976) Optimal foraging; the marginal value theorem. Theor Pop Biol 9:129–136

    Article  CAS  Google Scholar 

  • Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366

    Article  Google Scholar 

  • Connolly BM, Pearson DE, Mack RN (2014) Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95:1759–1769

    Article  CAS  PubMed  Google Scholar 

  • D’Anotonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87

    Article  Google Scholar 

  • US Climate Data (2018) https://www.usclimatedata.com/climate/tooele/utah/united-states/usut0254/2016/6. Accessed 14 May 2018

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London

    Book  Google Scholar 

  • Enge S, Nylund GM, Pavia H (2013) Native generalist herbivores promote invasion of a chemically defended seaweed via refuge-mediated apparent competition. Ecol Letters 16:487–492

    Article  Google Scholar 

  • Flake LD (1973) The food habits of four species of rodents on a short-grass prairie in Colorado. J Mammal 54:636–647

    Article  Google Scholar 

  • Griffith AB (2010) Positive effects of native shrubs on Bromus tectorum demography. Ecology 91:141–154

    Article  PubMed  Google Scholar 

  • Gross CL, Mackay D (2014) Two decades of demography reveals that seed and seedling transitions limit population persistence in a translocated shrub. Ann Bot 114:85–96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harper KT, Freeman DC, Ostler WK, Klikoff LG (1978) The flora of Great Basin mountain ranges: diversity, sources, and dispersal ecology. Gt Basin Nat Mem 2:81–103

    Google Scholar 

  • Hassan MA, West NE (1986) Dynamics of soil seed pools in burned and unburned sagebrush semi-deserts. Ecology 67:269–272

    Article  Google Scholar 

  • Hayssen V (1991) Dipodomys microps. Mammal Species 389:1–9

    Article  Google Scholar 

  • Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Pop Biol 12:197–229

    Article  CAS  Google Scholar 

  • Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Perspect Plant Ecol 1:32–46

    Article  Google Scholar 

  • Humphrey LD, Schupp EW (2001) Seed banks of Bromus tectorum-dominated communities in the Great Basin. West North Am Nat 61:85–92

    Google Scholar 

  • Jogesh T, Carpenter D, Cappuccino N (2008) Herbivory on invasive exotic plants and their non-invasive relatives. Biol Invasions 10:797–804

    Article  Google Scholar 

  • Jones WT (1989) Dispersal distance and the range of nightly movement in Merriam’s kangaroo rats. J Mammal 70:27–34

    Article  Google Scholar 

  • Kamil AC, Balda RP (1985) Cache recovery and spatial memory in Clark’s nutcracker (Nucifraga colombiana). J Exp Psychol Anim Behav Process 11:95–111

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kelrick MI, MacMahon JA (1985) Nutritional and physical attributes of seeds of some common sagebrush-steppe plants: some implications for ecological theory and management. J Range Manag 38:65–69

    Article  Google Scholar 

  • Kelrick MI, MacMahon JA, Parmenter RR, Sisson DV (1986) Native seed preferences of shrub-steppe rodents, birds and ants: the relationships of seed attributes and seed use. Oecologia 68:327–337

    Article  CAS  PubMed  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest Package: tests in linear mixed effects models. J Stat Softw 82:1–26

    Article  Google Scholar 

  • Larios L, Pearson DE, Maron JL (2017) Incorporating the effects of generalist seed predators into plant community theory. Funct Ecol 31:1856–1867

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Longland WS, Jenkins SH, Vander Wall SB, Veech JA, Pyare S (2001) Seedling recruitment in Oryzopsis hymenoides: are desert granivores mutualists or predators? Ecology 82:3131–3148

    Article  Google Scholar 

  • Louda SM (1982) Distribution ecology: variation in plant recruitment over a gradient in relation to insect seed predation. Ecol Monogr 52:25–41

    Article  Google Scholar 

  • Louda SM (1989) Predation in the dynamics of seed regeneration. In: Leck MA, Parker VT, Simpson RL (eds) Ecology of soil seed banks. Academic Press, San Diego, pp 25–51

    Chapter  Google Scholar 

  • Lucero JE (2017) A biogeographic perspective on the impacts and importance of rodent granivory on native vs. invasive plants. Dissertation, The University of Montana

  • Lucero JE, Allen PS, McMillan BR (2015) Increased primary production from an exotic invader does not subsidize native rodents. PLoS ONE 10(8):e0131564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacMahon JA, Mull JF, Crist TO (2000) Harvester ants (Pogonomyrmex spp.): their community and ecosystem influences. Annu Rev Ecol Syst 31:265–291

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Maron JL, Kauffman M (2006) Habitat-specific consumer impacts on plant population dynamics. Ecology 87:113–124

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Maron JL, Pearson DE, Potter T, Ortega Y (2012) Seed size and provenance mediate the joint effects of disturbance and seed predation on community assembly. J Ecol 100:1492–1500

    Article  Google Scholar 

  • Meyer SE, Allen PS (2009) Predicting seed dormancy loss and germination timing in a semiarid environment using hydrothermal time models. Seed Sci Res 19:225–240

    Article  Google Scholar 

  • Norton U, Mosier AR, Morgan JA, Derner JD, Ingram JL, Stahl PD (2008) Moisture pulses, trace gas emissions and soil C and N in cheatgrass and native grass-dominated sagebrush-steppe in Wyoming, USA. Soil Biol Biochem 40:1421–1431

    Article  CAS  Google Scholar 

  • O’Farrell MJ (1978) Home range dynamics of rodents in a sagebrush community. J Mammal 59:657–668

    Article  Google Scholar 

  • Orrock JL, Witter MS, Reichman OJ (2008) Apparent competition with an exotic plant reduces native plant establishment. Ecology 89:1168–1174

    Article  PubMed  Google Scholar 

  • Ostoja SM, Schupp EW (2009) Conversion of sagebrush shrublands to exotic annual grasslands negatively impacts small mammal communities. Divers Distrib 15:863–870

    Article  Google Scholar 

  • Ostoja SM, Schupp EW, Durham S, Klinger R (2013) Seed harvesting is influenced by associational effects in mixed seed neighbourhoods, not just by seed density. Funct Ecol 27:775–785

    Article  Google Scholar 

  • Paine CET, Beck H, Terborgh J (2016) How mammalian predation contributes to tropical tree community structure. Ecology 97:3326–3336

    Article  PubMed  Google Scholar 

  • Pearson DE, Callaway RM (2008) Weed-control insects reduce native-plant recruitment through second-order apparent competition. Ecol Appl 18:1489–1500

    Article  PubMed  Google Scholar 

  • Pearson DE, Callaway RM, Maron JL (2011) Biotic resistance via granivory: establishment by invasive, naturalized, and native asters reflects generalist preference. Ecology 92:1748–1757

    Article  PubMed  Google Scholar 

  • Pearson DE, Ortega YK, Ozkan E, Hierro JL (2015) Quantifying “apparent” impact and distinguishing impact from invasiveness in multispecies plant invasions. Ecol Appl 26:162–173

    Article  Google Scholar 

  • Pearson DE, Eren O, Ortega YK, Villareal D, Sentürk M, Miguel MF, Weinzettel CM, Prina A, Hierro JL (2017) Are exotic plants more abundant in the introduced versus native range? J Ecol 00:1–10

    Google Scholar 

  • Pulliam HR (1974) On the theory of optimal diets. Am Nat 108:59–74

    Article  Google Scholar 

  • R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reader RJ (1993) Control of seedling emergence by ground cover and seed predation in relation to seed size for some oldfield species. J Ecol 81:169–175

    Article  Google Scholar 

  • Rehmeier RL, Kaufman GA, Kaufman DW (2004) Long distance movements of the deer mouse in tallgrass prairie. J Mammal 85:562–568

    Article  Google Scholar 

  • Rose KE, Louda SM, Rees M (2005) Demographic and evolutionary impacts of native and invasive insect herbivores on Cirsium canescens. Ecology 86:453–465

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful for funding from the Montana Institute on Ecosystems, the National Science Foundation Established Program to Stimulate Competitive Research Track-1 EPS-1101342 (INSTEP 3), the Organismal Biology and Ecology Program at The University of Montana, and the American Museum of Natural History. We also thank Dean Pearson and John Maron for insightful comments that improved our work.

Author information

Authors and Affiliations

  1. Division of Biological Sciences and the Institute on Ecosystems, The University of Montana, Missoula, MT, 59812, USA

    Jacob E. Lucero & Ragan M. Callaway

Authors
  1. Jacob E. Lucero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ragan M. Callaway
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jacob E. Lucero.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lucero, J.E., Callaway, R.M. Native granivores reduce the establishment of native grasses but not invasive Bromus tectorum. Biol Invasions 20, 3491–3497 (2018). https://doi.org/10.1007/s10530-018-1789-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-018-1789-x

Keywords

Search

Navigation