Plant Ecology

, Volume 219, Issue 9, pp 1053–1061 | Cite as

Do seeds from invasive bromes experience less granivory than seeds from native congeners in the Great Basin Desert?

  • Jacob E. LuceroEmail author


In part, the enemy release hypothesis of plant invasion posits that generalist herbivores in the non-native ranges of invasive plants will prefer native plants to exotic invaders. However, the extent to which this occurs in natural communities is unclear. Here, I examined the foraging preferences of an important guild of generalist herbivores—granivorous rodents—with respect to seeds from a suite of native and invasive Bromus (“brome”) species at five study sites distributed across ≈ 80,000 km2 of the Great Basin Desert, USA. By examining only congeners, I accounted for a potentially large source of interspecific variation (phylogenetic relatedness). In general, granivorous rodents removed seeds from native bromes at a 23% higher rate than seeds from invasive bromes, suggesting a preference for native species. This preference was not entirely explained by seed size, and patterns of seed removal were consistent across study sites. These findings suggest that invasive bromes in the Great Basin might experience less rodent granivory than native congeners, which is consistent with a key prediction derived from the enemy release hypothesis.


Bromus Enemy release hypothesis Generalist herbivores Granivory Great Basin Rodents 



I am grateful for funding from task agreement P14AC00728 between the National Park Service and the Ragan M. Callaway Lab at the University of Montana, the Montana Institute on Ecosystems, National Science Foundation Established Program to Stimulate Competitive Research Track-1 EPS-1101342 (INSTEP 3), and the Organismal Biology and Ecology Program at the University of Montana. I especially thank Ray Callaway for his excellent guidance and feedback.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11258_2018_858_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 13 kb)


  1. Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715CrossRefGoogle Scholar
  2. Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? an experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86:2979–2989CrossRefGoogle Scholar
  3. Baayan RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412CrossRefGoogle Scholar
  4. 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 9:173–183CrossRefGoogle Scholar
  5. Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Syst 40:1–20CrossRefGoogle Scholar
  6. Besaw L, Thelen G, Sutherland S, Metlen K, Callaway RM (2011) Disturbance, resource pulses, and invasion: short-term shifts in competitive effects, not growth responses, favor exotic annuals. J Appl Ecol 48:998–1006CrossRefGoogle Scholar
  7. Blackwell TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefGoogle Scholar
  8. Blaney CS, Kotanen PM (2001) Post-dispersal losses to seed predators: an experimental comparison of native and exotic old field plants. Can J Bot 79:284–292Google Scholar
  9. Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895CrossRefPubMedGoogle Scholar
  10. Bowman TRS, McMillan BR, St. Clair SB (2017) Rodent herbivory and fire differentially affect plant species recruitment based on variability in life history traits. Ecosphere 8:1–10Google Scholar
  11. Brown JH, Reichman OJ, Davidson DW (1979) Granivory in desert ecosystems. Ann Rev Ecol Syst 10:201–227CrossRefGoogle Scholar
  12. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523CrossRefPubMedGoogle Scholar
  13. Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438CrossRefPubMedPubMedCentralGoogle Scholar
  14. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40CrossRefGoogle Scholar
  15. Connolly BM, Pearson DE, Mack RN (2014) Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95:1759–1769CrossRefPubMedGoogle Scholar
  16. D’Anotonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Ann Rev Ecol Syst 23:63–87CrossRefGoogle Scholar
  17. Daws MI, Hall J, Flynn S, Pritchard HW (2007) Do invasive species have bigger seeds? Evidence from intra- and inter-specific comparisons. S Afr J Bot 73:138–143CrossRefGoogle Scholar
  18. DeWalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483CrossRefGoogle Scholar
  19. Dillemuth FP, Rietschier EA, Cronin JT (2009) Patch dynamics of a native grass in relation to the spread of invasive smooth brome (Bromus inermis). Biol Invasions 11:1381–1391CrossRefGoogle Scholar
  20. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  21. Enge S, Nylund GM, Pavia H (2013) Native generalist herbivores promote invasion of a chemically defended seaweed via refuge-mediated apparent competition. Ecol Lett 16:487–492CrossRefPubMedGoogle Scholar
  22. Flake LD (1973) The food habits of four species of rodents on a short-grass prairie in Colorado. J Mammal 54:636–647CrossRefGoogle Scholar
  23. Gallagher RV, Randall RP, Leishman MR (2014) Trait differences between naturalized and invasive plant species independent of residence time and phylogeny. Conserv Biol 2:360–369Google Scholar
  24. Germino MJ, Chambers JC, Brown CS (2016) Exotic brome-grasses in arid and semiarid ecosystems of the western US: causes, consequences, and management implications. Springer International Publishing, New YorkCrossRefGoogle Scholar
  25. Harper KT, Freeman DC, Ostler WK, Klikoff LG (1978) The flora of Great Basin mountain ranges: diversity, sources, and dispersal ecology. Great Basin Nat Mem 2:81–103Google Scholar
  26. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Pop Biol 12:197–229CrossRefGoogle Scholar
  27. Holt RD, Kotler BP (1987) Short-term apparent competition. Am Nat 130:412–430CrossRefGoogle Scholar
  28. Hoset KS, Kyro K, Oksanen T, Oksanen L, Olofsson J (2014) Spatial variation in vegetation damage relative to primary productivity, small rodent abundance and predation. Ecography 37:894–901CrossRefGoogle Scholar
  29. Humphrey LD, Schupp EW (2004) Seed banks of Bromus tectorum-dominated communities in the Great Basin. West North Am Nat 61:85–92Google Scholar
  30. Jones WT (1989) Dispersal distance and the range of nightly movement in Merriam’s kangaroo rats. J Mamm 70:27–34CrossRefGoogle Scholar
  31. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  32. Kelrick MI, MacMahon JA (1985) Nutritional and physical attributes of seeds of some common sage-steppe plants: some implications for ecological theory and management. J Range Manag 38:65–69CrossRefGoogle Scholar
  33. 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 68:327–337CrossRefPubMedGoogle Scholar
  34. Krebs JR, Erichsen JT, Webber MI, Charnov EL (1977) Optimal prey selection in the great tit (Parus major). Anim Behav 25:30–38CrossRefGoogle Scholar
  35. Lankau RA, Rodgers WE, Siemann E (2004) Constraints on the utilization of the invasive Chinese tallow tree Sapium sebiferum by generalist native herbivores in coastal prairies. Ecol Entomology 29:66–75CrossRefGoogle Scholar
  36. Larios L, Pearson DE, Maron JL (2017) Incorporating the effects of generalist seed predators into plant community theory. Funct Ecol 31:1856–1867CrossRefGoogle Scholar
  37. Lieurance D, Cipollini D (2013) Exotic Lonicera species both escape and resist specialist and generalist herbivores in the introduced range in North America. Biol Invasions 15:1713–1724CrossRefGoogle Scholar
  38. Liu H, Stilling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545CrossRefGoogle Scholar
  39. Lucero JE (2017) A biogeographic perspective on the impacts and importance of rodent granivory on native vs. invasive plants. Dissertation, The University of MontanaGoogle Scholar
  40. Lucero JE, Callaway RM (2018) Native granivores reduce the establishment of native grasses but not invasive Bromus tectorum. Biol Invasions. CrossRefGoogle Scholar
  41. Lucero JE, Allen PS, McMillan BR (2015) Increased primary production from an exotic invader does not subsidize native rodents. PLoS ONE 10:e0131564CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mack RN (1981) Invasion of Bromus tectorum L. into western North America: an ecological chronicle. Agro-Ecosyst 7:145–165CrossRefGoogle Scholar
  43. MacMahon JA, Mull JF, Crist TO (2000) Harvester ants (Pogonomyrmex spp.): their community and ecosystem influences. Ann Rev Ecol Syst 31:265–291CrossRefGoogle Scholar
  44. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B 273:2575–2584CrossRefPubMedGoogle Scholar
  45. Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373CrossRefGoogle Scholar
  46. 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 100:1492–1500CrossRefGoogle Scholar
  47. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WL, Parker IM, Power AG, Seabloom EW, Torchin ME, Vasquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:729–740CrossRefGoogle Scholar
  48. Morrison WE, Hay ME (2011) Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PLoS ONE 6:e17227CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 40:1421–1431CrossRefGoogle Scholar
  50. Novoa A, Rodriguez J, Lopez-Nogueira A, Richardson DM, Gonzalez L (2016) Seed characteristics in Cactaceae: useful diagnostic features for screening species for invasiveness? S Afr J Bot 105:61–65CrossRefGoogle Scholar
  51. O’Farrell MJ (1978) Home range dynamics of rodents in a sagebrush community. J Mamm 59:657–668CrossRefGoogle Scholar
  52. Ostoja SM, Schupp EW (2009) Conversion of sagebrush shrublands to exotic annual grasslands negatively impacts small mammal communities. Divers Distrib 15:863–870CrossRefGoogle Scholar
  53. 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 27:775–785CrossRefGoogle Scholar
  54. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  55. Parkinson H, Zabinski C, Shaw N (2013) Impact of native grasses and cheatgrass (Bromus tectorum) on Great Basin forb and seedling growth. Rangel Ecol Manag 66:174–180CrossRefGoogle Scholar
  56. Pearson DE, Callaway RM, Maron JL (2011) Biotic resistance via granivory: establishment by invasive, naturalized, and native asters reflects generalist preference. Ecology 92:1748–1757CrossRefPubMedGoogle Scholar
  57. Pearson DE, Ortega YK, Ozkan E, Hierro JL (2016) Quantifying “apparent” impact and distinguishing impact from invasiveness in multispecies plant invasions. Ecol Appl 26:162–173CrossRefPubMedGoogle Scholar
  58. Phillips ML, Murray BR (2012) Invasiveness in exotic plant species is linked to high seed survival in the soil. Evol Ecol Res 14:83–94Google Scholar
  59. Pulliam HR (1974) On the theory of optimal diets. Am Nat 108:59–74CrossRefGoogle Scholar
  60. R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  61. Reader RJ (1993) Control of seedling emergence by ground cover and seed predation in relation to seed size for some old-field species. J Ecol 81:169–175CrossRefGoogle Scholar
  62. Salo LF (2005) Red brome (Bromus rubens subsp. madritensis) in North America: possible modes for early introductions, subsequent spread. Biol Invasions 7:165–180CrossRefGoogle Scholar
  63. Schaffner U, Ridenour WM, Wolf VC, Bassett T, Muller C, Muller-Scharer H, Sutherland S, Lortie CJ, Callaway RM (2011) Plant invasions, generalist herbivores, and novel defense weapons. Ecology 92:829–835CrossRefPubMedGoogle Scholar
  64. Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190CrossRefGoogle Scholar
  65. Turnbull LA, Rees M, Crawley MJ (1999) Seed mass and the competition/colonization trade-off: a sowing experiment. J Ecol 84:899–912CrossRefGoogle Scholar
  66. Underwood N, Inouye BD, Hamback PA (2014) A conceptual framework for associational effects: when do neighbors matter and how would we know? Q Rev Biol 89:1–19CrossRefPubMedGoogle Scholar
  67. Vasquez E, Sheley R, Svejcar T (2008) Nitrogen enhances the competitive ability of cheatgrass (Bromus tectorum) relative to native grasses. Invasive Plant Sci Manag 1:287–295CrossRefGoogle Scholar
  68. Vermeij MJA, Smith TB, Dailer ML, Smith CM (2009) Release from native herbivores facilitates the persistence of invasive marine algae: a biogeographical comparison of the relative contribution of nutrients and herbivory to invasion success. Biol Invasions 11:1463–1474CrossRefGoogle Scholar
  69. Williams JL, Crone EE (2006) The impact of invasive grasses on the population growth of Anemone patens, a long-lived native forb. Ecology 87:3200–3208CrossRefPubMedGoogle Scholar
  70. Williams JL, Auge H, Maron JL (2010) Testing hypotheses for exotic plant success: parallel experiments in the native and introduced ranges. Ecology 91:1355–1366CrossRefPubMedGoogle Scholar
  71. Wulff RD (1986) Seed size variation in Desmodium paniculatum: III. Effects on reproductive yield and competitive ability. J Ecol 74:115–121CrossRefGoogle Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Division of Biological Sciences and the Institute on EcosystemsUniversity of MontanaMissoulaUSA

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