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Oecologia

, Volume 185, Issue 3, pp 465–473 | Cite as

Rodent herbivory differentially affects mortality rates of 14 native plant species with contrasting life history and growth form traits

  • Tiffanny R. Sharp Bowman
  • Brock R. McMillan
  • Samuel B. St. Clair
Community ecology – original research

Abstract

Ecosystems are transformed by changes in disturbance regimes including wildfire and herbivory. Rodent consumers can have strong top-down effects on plant community assembly through seed predation, but their impacts on post-germination seedling establishment via seedling herbivory need better characterization, particularly in deserts. To test the legacy effects of fire history, and native rodent consumers on seedling establishment, we evaluated factorial combinations of experimental exclusion of rodents and fire history (burned vs. unburned) on seedling survival of 14 native plant species that vary in their life history strategies and growth form in the Mojave Desert. Seedlings were placed into the experimental plots, and seedling survival was monitored daily for 8 days. The legacy effects of fire history had minimal effects on seedling survival, but rodent exclusion, year, and their interaction were strongly significant. Seedling survival rates were nearly sixfold greater in rodent exclusion plots compared to control plots in 2012 (53 vs. 9%) and 17-fold greater in 2013 (17 vs. 1%). The dramatic increase in seedling mortality from 2012 to 2013 was likely driven by an increase in rodent abundance and an outbreak of grasshoppers that appears to have intensified the rodent effect. There was strong variability in plant species survival in response to rodent herbivory with annual plants and forb species showing lower survival than perennial plants and shrub species. These results indicate that rodent consumers can strongly regulate seedling survival of native plant species with potentially strong regulatory effects on plant community development.

Keywords

Consumers Disturbance Fire Small mammal Desert 

Notes

Acknowledgements

Many thanks to Rachel Giannetta and Brandon White for assistance in the field and to Dr. Randy Larson who advised on the data analysis. The BLM and Brigham Young University’s Lytle Ranch Preserve provided access to study sites. The BLM also provided NEPA clearance and conducted the controlled burns. This project was funded by USDA NIFA Grant: 2010-38415-21908.

Author contribution statement

SBS and BRM conceived and designed the experiments. TRSB performed the experiments. TRSB and SBS analyzed the data. SBS and TRSB wrote the manuscript; BRM provided editorial advice.

Supplementary material

442_2017_3944_MOESM1_ESM.docx (2.7 mb)
Supplementary material 1 (DOCX 2793 kb)

References

  1. Abbott LB, Roundy BA (2003) Available water influences field germination and recruitment of seeded grasses. J Range Manag 56:56–64. doi: 10.2307/4003882 CrossRefGoogle Scholar
  2. Barton KE, Hanley ME (2013) Seedling herbivore interactions: insights into plant defence and regeneration patterns. Ann Bot 112:643–650. doi: 10.1093/aob/mct139 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beatley JC (1976) Environments of kangaroo rats (Dipodomys) and effects of environmental change on populations in southern Nevada. J Mammal 57:67–93CrossRefGoogle Scholar
  4. Beck MJ, Vander Wall SB (2010) Seed dispersal by scatter-hoarding rodents in arid environments. J Ecol 98:1300–1309CrossRefGoogle Scholar
  5. Bestelmeyer BT, Kalil NI, Peters DPC (2007) Does shrub invasion indirectly limit grass establishment via seedling herbivory? A test at grassland-shrubland ecotones. J Veg Sci 18:363–370. doi:10.1658/1100-9233(2007)18[363:dsiilg]2.0.co;2Google Scholar
  6. Bowman D et al (2009) Fire in the earth system. Science 324:481–484. doi: 10.1126/science.1163886 CrossRefPubMedGoogle Scholar
  7. Bowman D et al (2011) The human dimension of fire regimes on Earth. J Biogeogr 38:2223–2236. doi: 10.1111/j.1365-2699.2011.02595.x CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brooks ML, Matchett JR (2006) Spatial and temporal patterns of wildfires in the Mojave Desert, 1980–2004. J Arid Environ 67:148–164CrossRefGoogle Scholar
  9. Brown JH, Heske EJ (1990a) Control of a desert-grassland transition by a keystone rodent guild. Science 250:1705–1707CrossRefPubMedGoogle Scholar
  10. Brown JH, Heske EJ (1990b) Temporal changes in a Chihuahuan Desert rodent community. Oikos 59:290–302. doi: 10.2307/3545139 CrossRefGoogle Scholar
  11. Bukowski BE, Baker WL (2013) Historical fire regimes, reconstructed from land-survey data, led to complexity and fluctuation in sagebrush landscapes. Ecol Appl 23:546–564CrossRefPubMedGoogle Scholar
  12. Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367. doi: 10.1111/j.1365-2435.2010.01794.x CrossRefGoogle Scholar
  13. Daly M, Behrends PR, Wilson MI, Jacobs LF (1992) Behavioral modulation of predation risk—moonlight avoidance and crepuscular compensation in a nocturnal desert rodent Dipodomys merriami. Anim Behav 44:1–9. doi: 10.1016/s0003-3472(05)80748-1 CrossRefGoogle Scholar
  14. Duval BD, Jackson E, Whitford WG (2005) Mesquite (Prosopis glandulosa) germination and survival in black-grama (Bouteloua eriopoda) grassland: relations between microsite and heteromyid rodent (Dipodomys spp.) impact. J Arid Environ 62:541–554. doi: 10.1016/j.jaridenv.2005.01.012 CrossRefGoogle Scholar
  15. Eiswerth ME, Shonkwiler JS (2006) Examining post-wildfire reseeding on and rangeland: a multivariate tobit modelling approach. Ecol Model 192:286–298. doi: 10.1016/j.ecolmodel.2005.07.003 CrossRefGoogle Scholar
  16. Eiswerth ME, Krauter K, Swanson SR, Zielinski M (2009) Post-fire seeding on Wyoming big sagebrush ecological sites: regression analyses of seeded nonnative and native species densities. J Environ Manag 90:1320–1325. doi: 10.1016/j.jenvman.2008.07.009 CrossRefGoogle Scholar
  17. Falkenberg JC, Clarke JA (1998) Microhabitat use of deer mice: effects of interspecific interaction risks. J Mammal 79:558–565. doi: 10.2307/1382986 CrossRefGoogle Scholar
  18. Flake L (1973) Food habits of four species of rodents in a short grass prairie in Colo. J Mammal 54:636–647CrossRefGoogle Scholar
  19. Freeman ED, Sharp TR, Larsen RT, Knight RN, Slater SJ, McMillan BR (2014) Negative effects of an exotic grass invasion on small-mammal communities. PLoS One. doi: 10.1371/journal.pone.0108843 Google Scholar
  20. Groves CR, Steenhof K (1988) Responses of small mammals and vegetation to wildfire in shadscale communities in southwestern Idaho. Northwest Sci 62:205–210Google Scholar
  21. Horn KJ, St. Clair SB (2017) Wildfire and exotic grass invasion alter plant productivity in response to climate variability in the Mojave Desert. Landsc Ecol 32:635–646. doi: 10.1007/s10980-016-0466-7 CrossRefGoogle Scholar
  22. Horn KJ, McMillan BR, St. Clair SB (2012) Expansive fire in Mojave Desert shrubland reduces abundance and species diversity of small mammals. J Arid Environ 77:54–58. doi: 10.1016/j.jaridenv.2011.10.003 CrossRefGoogle Scholar
  23. Horn KJ, Wilkinson J, White S, St. Clair SB (2015) Desert wildfire impacts on plant community function. Plant Ecol 216:1623–1634. doi: 10.1007/s11258-015-0546-9 CrossRefGoogle Scholar
  24. Howe HF, Lane D (2004) Vole-driven succession in experimental wet-prairie restorations. Ecol Appl 14:1295–1305. doi: 10.1890/03-5182 CrossRefGoogle Scholar
  25. Hulme PE (1994) Seedling herbivory in grasslands—relative impact of vertebrate and invertebrate herbivores. J Ecol 82:873–880. doi: 10.2307/2261451 CrossRefGoogle Scholar
  26. Jacquemyn H, Brys R, Neubert MG (2005) Fire increases invasive spread of Molinia caerulea mainly through changes in demographic parameters. Ecol Appl 15:2097–2108. doi: 10.1890/04-1762 CrossRefGoogle Scholar
  27. Jameson EW (1952) Food of deer mice, Peromyscus maniculatus and P. Boylei, in the northern Sierra Nevada, California. J Mammal 33:50–60. doi: 10.2307/1375640 CrossRefGoogle Scholar
  28. Knutson KC et al (2014) Long-term effects of seeding after wildfire on vegetation in Great Basin shrubland ecosystems. J Appl Ecol 51:1414–1424. doi: 10.1111/1365-2664.12309 CrossRefGoogle Scholar
  29. Kotler BP (1984) Risk of predation and the structure of desert rodent communities. Ecology 65:689–701. doi: 10.2307/1938041 CrossRefGoogle Scholar
  30. Lenth RV (2014) lsmeans: least-squares meansGoogle Scholar
  31. Lindroth RL, St. Clair SB (2013) Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores. For Ecol Manag 299:14–21. doi: 10.1016/j.foreco.2012.11.018 CrossRefGoogle Scholar
  32. Longland WS, Ostoja SM (2013) Ecosystem services from keystone species: diversionary seeding and seed-caching Desert Rodents can enhance Indian ricegrass seedling establishment. Restor Ecol 21:285–291. doi: 10.1111/j.1526-100X.2012.00895.x CrossRefGoogle Scholar
  33. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc Biol Sci Ser B 273:2575–2584. doi: 10.1098/rspb.2006.3587 CrossRefGoogle Scholar
  34. Maron JL, Kauffman MJ (2006) Habitat-specific impacts of multiple consumers on plant population dynamics. Ecology 87:113–124. doi: 10.1890/05-0434 CrossRefPubMedGoogle Scholar
  35. Maron JL, Pearson DE, Potter T, Ortega YK (2012) Seed size and provenance mediate the joint effects of disturbance and seed predation on community assembly. J Ecol 100:1492–1500. doi: 10.1111/j.1365-2745.2012.02027.x CrossRefGoogle Scholar
  36. Meyer SE, Pendleton BK (2005) Factors affecting seed germination and seedling establishment of a long-lived desert shrub (Coleogyne ramosissima: rosaceae). Plant Ecol 178:171–187. doi: 10.1007/s11258-004-3038-x CrossRefGoogle Scholar
  37. Monasmith TJ, Demarais S, Root JJ, Britton CM (2010) Short-term fire effects on small mammal populations and vegetation of the northern Chihuahuan Desert. Int J Ecol 2010:9CrossRefGoogle Scholar
  38. Ostoja SM, Schupp EW (2009) Conversion of sagebrush shrublands to exotic annual grasslands negatively impacts small mammal communities. Divers Distrib 15:863–870. doi: 10.1111/j.1472-4642.2009.00593.x CrossRefGoogle Scholar
  39. 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
  40. Pearson DE, Hierro JL, Chiuffo M, Villarreal D (2014) Rodent seed predation as a biotic filter influencing exotic plant abundance and distribution. Biol Invasions 16:1185–1196. doi: 10.1007/s10530-013-0573-1 CrossRefGoogle Scholar
  41. Pearson D, Ortega YK, Runyon J, Butler J (2015) Secondary invasion: the bane of weed management. Biol Conserv Rev 197:8–17CrossRefGoogle Scholar
  42. Perez-Harguindeguy N, Diaz S, Vendramini F, Cornelissen JHC, Gurvich DE, Cabido M (2003) Leaf traits and herbivore selection in the field and in cafeteria experiments. Austral Ecol 28:642–650. doi: 10.1046/j.1442-9993.2003.01321.x CrossRefGoogle Scholar
  43. Perkins L, Bienek G, Klikoff L (1976) The diet of Dipodomys merriami vulcani. Am Midl Nat 95:507–512CrossRefGoogle Scholar
  44. Pyke DA (1986) Demographic responses of Bromus tectorum and seedlings of Agropyron spicatum to grazing by small mammals—occurrence and severity of grazing. J Ecol 74:739–754. doi: 10.2307/2260395 CrossRefGoogle Scholar
  45. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. Rosenzweig ML, Winakur J (1969) Population ecology of desert rodent communities: habitats and environmental complexity. Ecology 50:558–572CrossRefGoogle Scholar
  47. Sharp Bowman T (2015) The cascading effects of invasive grasses in North American deserrts: the interactions of fire, plants and small mammals. MS, Brigham Young University, ProvoGoogle Scholar
  48. Simons LH (1991) Rodent dynamics in relation to fire in the Sonoran Desert. J Mammal 72:518–524CrossRefGoogle Scholar
  49. Sipos MP, Andersen MC, Whitford WG, Gould WR (2002) Graminivory by Dipodomys ordii and Dipodomys merriami on four species of perennial grasses. Southwest Nat 47:276–281. doi: 10.2307/3672915 CrossRefGoogle Scholar
  50. Sorensen JS, Heward E, Dearing MD (2005) Plant secondary metabolites alter the feeding patterns of a mammalian herbivore (Neotoma lepida). Oecologia 146:415–422. doi: 10.1007/s00442-005-0236-8 CrossRefPubMedGoogle Scholar
  51. St. Clair 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. doi: 10.1002/ecy.1391 CrossRefPubMedGoogle Scholar
  52. Therneau T (2012a) Coxme: mixed effects Cox models. https://cran.r-project.org/web/packages/coxme/vignettes/coxme.pdf. Accessed 5 Jan 2017
  53. Therneau T (2012b) A package for survival analysis in S. https://cran.r-project.org/package=survival. Accessed 5 Jan 2017
  54. Villalba JJ, Burritt EA, St. Clair SB (2014) Aspen (Populus tremuloides Michx.) intake and preference by mammalian herbivores: the role of plant secondary compounds and nutritional context. J Chem Ecol 40:1135–1145. doi: 10.1007/s10886-014-0507-0 CrossRefPubMedGoogle Scholar
  55. Wan HY, Rhodes AC, St. Clair SB (2014) Fire severity alters plant regeneration patterns and defense against herbivores in mixed aspen forests. Oikos 123:1479–1488. doi: 10.1111/oik.01521 CrossRefGoogle Scholar
  56. Went FW, Westergaard M (1949) Ecology of desert plants. 3 Development of plants in the Death Valley National Monument. Calif Ecol 30:26–38. doi: 10.2307/1932275 CrossRefGoogle Scholar
  57. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. doi: 10.1111/j.2041-210X.2009.00001.x CrossRefGoogle Scholar
  58. Zwolak R, Pearson DE, Ortega YK, Crone EE (2010) Fire and mice: seed predation moderates fire’s influence on conifer recruitment. Ecology 91:1124–1131. doi: 10.1890/09-0332.1 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of Plant and Wildlife SciencesBrigham Young UniversityProvoUSA

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