Skip to main content

Advertisement

SpringerLink
Log in

Gopher mounds decrease nutrient cycling rates and increase adjacent vegetation in volcanic primary succession

  • Ecosystem ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Fossorial mammals may affect nutrient dynamics and vegetation in recently initiated primary successional ecosystems differently than in more developed systems because of strong C and N limitation to primary productivity and microbial communities. We investigated northern pocket gopher (Thomomys talpoides) effects on soil nutrient dynamics, soil physical properties, and plant communities on surfaces created by Mount St. Helens’ 1980 eruption. For comparison to later successional systems, we summarized published studies on gopher effects on soil C and N and plant communities. In 2010, 18 years after gopher colonization, we found that gophers were active in ~2.5 % of the study area and formed ~328 mounds ha−1. Mounds exhibited decreased species density compared to undisturbed areas, while plant abundance on mound margins increased 77 %. Plant burial increased total soil carbon (TC) by 13 % and nitrogen (TN) by 11 %, compared to undisturbed soils. Mound crusts decreased water infiltration, likely explaining the lack of detectable increases in rates of NO3–N, NH4–N or PO4–P leaching out of the rooting zone or in CO2 flux rates. We concluded that plant burial and reduced infiltration on gopher mounds may accelerate soil carbon accumulation, facilitate vegetation development at mound edges through resource concentration and competitive release, and increase small-scale heterogeneity of soils and communities across substantial sections of the primary successional landscape. Our review indicated that increases in TC, TN and plant density at mound margins contrasted with later successional systems, likely due to differences in physical effects and microbial resources between primary successional and older systems.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agren G, Bosatta E, Magill A (2001) Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128:94–98

    Article  Google Scholar 

  • Amundson R, Jenny H (1997) On a state factor model of ecosystems. BioScience 47:536–543

    Article  Google Scholar 

  • Andersen DC, MacMahon JA (1985) Plant succession following the Mount St. Helens volcanic eruption: facilitation by a burrowing rodent, Thomomys talpoides. Am Midl Nat 114:62–69

    Article  Google Scholar 

  • Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545

    Article  CAS  PubMed  Google Scholar 

  • Bach CE (1994) Effects of a specialist herbivore (Altica subplicata) on Salix cordata and sand dune succession. Ecol Monogr 64:423–445

    Article  Google Scholar 

  • Belsley D, Kuh E, Welsch R (2004) Regression diagnostics: identifying influential data and sources of collinearity. Wiley series in probability and statistics. Wiley-Interscience, NY

    Google Scholar 

  • Bishop JG, Fagan WF, Schade JD, Crisafulli CM (2005) Causes and consequences of herbivory on prairie lupine (Lupinus lepidus) in early primary succession. In: Dale VH, Swanson F, Crisafulli CM (eds) Ecological responses to the 1980 eruptions of Mount St. Helens. Springer, Berlin, pp 151–161

    Chapter  Google Scholar 

  • Butler LG, Kielland K (2008) Acceleration of vegetation turnover and element cycling by mammalian herbivory in riparian ecosystems. J Ecol 96:136–144

    Google Scholar 

  • Canals RM, Herman DJ, Firestone MK (2003) How disturbance by fossorial mammals alters N cycling in a California annual grassland. Ecology 84:875–881

    Article  Google Scholar 

  • Carreiro M, Sinsabaugh R, Repert D, Parkhurst D (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365

    Article  Google Scholar 

  • Case MF, Halpern CB, Levin SA (2013) Contributions of gopher mound and casting disturbances to plant community structure in a Cascade Range meadow complex. Botany 91(91):555–561

    Article  Google Scholar 

  • Chapin FS (2002) Principles of terrestrial ecosystem ecology. Springer, New York

    Google Scholar 

  • Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618

    Article  CAS  PubMed  Google Scholar 

  • Collins BD, Dunne T (1986) Erosion of tephra from the 1980 eruption of Mount St. Helens. Geol Surv Am Bull 97:896–905

    Article  Google Scholar 

  • Collins BD, Dunne T (1988) Effects of forest land management on erosion and revegetation after the eruption of Mount St. Helens. Earth Surf Process Landf 13:193–205

    Article  Google Scholar 

  • Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21

    Article  Google Scholar 

  • Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119

    Article  Google Scholar 

  • Cortinas MR, Seastedt TR (1996) Short- and long-term effects of gophers (Thomomys talpoides) on soil organic matter dynamics in alpine tundra. Pedobiologia 40:162–170

    Google Scholar 

  • Crisafulli CM, MacMahon JA, Parmenter RR (2005) Small mammal survival and colonization on the Mount St. Helens Volcano: 1980–2002. Ecological responses to the 1980 eruption of Mount St. Helens, pp 199–218

  • Dahlgren RA, Saigusa M, Ugolini FC (2004) The nature, properties and management of volcanic soils. Adv Agron 82:113–182

    Article  CAS  Google Scholar 

  • Dale VH, Adams WM (2003) Plant reestablishment 15 years after debris avalanche at Mount St. Helens, Washington. Sci Total Environ 313:101–113

    Article  CAS  PubMed  Google Scholar 

  • de Graaff MA, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064

    Article  PubMed  Google Scholar 

  • del Moral R, Thomason LA, Wenke AC, Lozanoff N, Abata MD (2012) Primary succession trajectories on pumice at Mount St. Helens, Washington. J Veg Sci 23:73–85

    Article  Google Scholar 

  • Eldridge DJ (2009) Badger (Taxidea taxus) mounds affect soil hydrological properties in a degraded shrub-steppe. Am Midl Nat 161:350–358

    Article  Google Scholar 

  • Eviner VT, Chapin FS III (2005) Selective gopher disturbance influences plant species effects on nitrogen cycling. Oikos 109:154–166

    Article  Google Scholar 

  • Fagan WF, Bishop JG, Schade JD (2004) Spatially structured herbivory and primary succession at Mount St. Helens: a role for nutrients? Ecol Entomol 29:398–409

    Article  Google Scholar 

  • Fagan WF, Lewis M, Neubert M, Aumann C, Apple JL, Bishop JG (2005) When can herbivores slow or reverse the spread of an invading plant? A test case from Mount St. Helens. Am Nat 166:669–685

    Article  PubMed  Google Scholar 

  • Franklin JF, MacMahon JA, Swaonson FJ, Sedell JR (1985) Ecosystem responses to the eruption of Mount St. Helens. Natl Geogr Res 1:198–216

    Google Scholar 

  • Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171

    Article  Google Scholar 

  • Gibson DJ (1989) Effects of animal disturbance on tallgrass prairie vegetation. Am Midl Nat 121:144–154

    Article  Google Scholar 

  • Gill RA, Boie JA, Bishop JG, Larsen L, Apple JL, Evans RD (2006) Linking community and ecosystem development on Mount Saint Helens. Oecologia 148:312–324

    Article  PubMed  Google Scholar 

  • Gotelli NJ, Ellison AM (2013) A primer of ecological statistics, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Gotelli NJ, Entsminger GL (2009) EcoSim: null models software for ecology. Acquired Intelligence Inc. & Kesey-Bear, Jericho. http://garyentsminger.com/ecosim.htm

  • Grant WE, French NR, Folse LJ Jr (1980) Effects of pocket gopher mounds on plant production in shortgrass prairie ecosystems. Southwest Nat 25:215–224

    Article  Google Scholar 

  • Grant WE, McBrayer JF (1981) Effect of mound formation by pocket gophers (Geomys bursarius) on old-field ecosystems. Pedobiologia 22:21–28

    Google Scholar 

  • Halvorson JJ, Smith JL (2009) Carbon and nitrogen accumulation and microbial activity in Mount St. Helens pyroclastic substrates after 25 years. Plant Soil 315:211–228

    Article  CAS  Google Scholar 

  • Halvorson JJ, Smith JL, Kennedy AC (2005) Lupine effects on soil development and function during early primary succession at Mount St. Helens. Ecological responses to the 1980 eruption of Mount St. Helens, pp 243–254

  • Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146

    Article  CAS  Google Scholar 

  • Hartway C, Steinberg EK (1997) The influence of pocket gopher disturbance on the distribution and diversity of plants in western Washington prairies. In: Dunn P, Ewing K (eds) South Puget Sound prairie landscapes. The Nature Conservancy of Washington, Seattle, pp 131–139

    Google Scholar 

  • Hobbs RJ, Mooney HA (1991) Effects of rainfall variability and gopher disturbance on serpentine annual grassland dynamics. Ecology 72:59–68

    Article  Google Scholar 

  • Houlton BZ, Wang Y-P, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–331

    Article  CAS  PubMed  Google Scholar 

  • Huntly N, Inouye R (1988) Pocket gophers in ecosystems: patterns and mechanisms. BioScience 38:786–793

    Article  Google Scholar 

  • Inouye RS, Huntly N, Wasley GA (1997) Effects of pocket gophers (Geomys bursarius) on microtopographic variation. J Mammal 78:1144–1148

    Article  Google Scholar 

  • Inouye RS, Huntly NJ, Tilman D, Tester JR (1987) Pocket gophers (Geomys bursarius), vegetation, and soil nitrogen along a successional sere in east central Minnesota. Oecologia 72:178–184

    Article  Google Scholar 

  • Jones CC, Halpern CB, Niederer J (2008) Plant succession on gopher mounds in western Cascade meadows: consequences for species diversity and heterogeneity. Am Midl Nat 159:275–286

    Article  Google Scholar 

  • Kerley GIH, Whitford WG, Kay FR (2004) Effects of pocket gophers on desert soils and vegetation. J Arid Environ 58:155–166

    Article  Google Scholar 

  • Kielland K, Bryant JP (1998) Moose herbivory in taiga: effects on biogeochemistry and vegetation dynamics in primary succession. Oikos 82:377–383

    Article  Google Scholar 

  • Koide RT, Huenneke LF, Mooney HA (1987) Gopher mound soil reduces growth and affects ion uptake of two annual grassland species. Oecologia 72:284–290

    Article  Google Scholar 

  • Kramer MG, Sanderman J, Chadwick OA, Chorover J, Vitousek PM (2012) Long-term carbon storage through retention of dissolved aromatic acids by reactive particles in soil. Glob Change Biol 18:2594–2605

    Article  Google Scholar 

  • Kyle GP, Kulmatiski A, Beard KH (2008) Influence of pocket gopher mounds on nonnative plant establishment in a shrubsteppe ecosystem. West N Am Nat 68:374–381

    Article  Google Scholar 

  • Lambers H, Bishop JG, Hopper SD, Laliberté E, Zúñiga-Feest A (2012) Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems. Ann Bot 110:329–348

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Laycock WA, Richardson BZ (1975) Long-term effects of pocket gopher control on vegetation and soils of a subalpine grassland. J Range Manag 28:458–462

    Article  Google Scholar 

  • Lichter J (2000) Colonization constraints during primary succession on coastal Lake Michigan sand dunes. J Ecol 88:825–839

    Article  Google Scholar 

  • Litaor MI, Mancinelli R, Halfpenny JC (1996) The influence of pocket gophers on the status of nutrients in Alpine soils. Geoderma 70:37–48

    Article  CAS  Google Scholar 

  • Marleau JN, Jin Y, Bishop JG, Fagan WF, Lewis M (2011) A stoichiometric model of early plant primary succession. Am Nat 177:233–245

    Article  PubMed  Google Scholar 

  • McDonough WT (1974) Revegetation of gopher mound on aspen range in Utah. Gt Basin Nat 34:267–275

    Google Scholar 

  • Phillips RP, Meier IC, Bernhardt ES, Grandy AS, Wickings K, Finzi AC (2012) Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol Lett 15:1042–1049

    Article  PubMed  Google Scholar 

  • Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B 44:81–99

    Article  Google Scholar 

  • Reader RJ, Buck J (1991) Community response to experimental soil disturbance in a midsuccessional, abandoned pasture. Vegetatio 92:151–159

    Google Scholar 

  • Reichman OJ, Bendix JH, Seastedt TR (1993) Distinct animal-generated edge effects in a tallgrass prairie community. Ecology 74:1281–1285

    Article  Google Scholar 

  • Reichman OJ, Seabloom EW (2002) The role of pocket gophers as subterranean ecosystem engineers. Trends Ecol Evol 17:44–49

    Article  Google Scholar 

  • Rogers WE, Hartnett DC (2001a) Temporal vegetation dynamics and recolonization mechanisms on different-sized soil disturbances in tallgrass prairie. Am J Bot 88:1634–1642

    Article  CAS  PubMed  Google Scholar 

  • Rogers WE, Hartnett DC (2001b) Vegetation responses to different spatial patterns of soil disturbance in burned and unburned tallgrass prairie. Plant Ecol 155:99–109

    Article  Google Scholar 

  • Rogers WE, Hartnett DC, Elder B (2001) Effects of plains pocket gopher (Geomys bursarius) disturbances on tallgrass-prairie plant community structure. Am Midl Nat 145:344–357

    Article  Google Scholar 

  • Rückamp D, Amelung W, Simone Borma Ld, Pena Naval L, Martius C (2009) Carbon and nutrient leaching from termite mounds inhabited by primary and secondary termites. Appl Soil Ecol 43:159–162

    Article  Google Scholar 

  • Seabloom E, Richards S (2003) Multiple stable equilibria in grasslands mediated by herbivore population dynamics and foraging behavior. Ecology 84:2891–2904

    Article  Google Scholar 

  • Sherrod SK, Seastedt TR (2001) Effects of the northern pocket gopher (Thomomys talpoides) on alpine soil characteristics, Niwot Ridge, CO. Biogeochemistry 55:195–218

    Article  CAS  Google Scholar 

  • Sherrod SK, Seastedt TR, Walker MD (2005) Northern pocket gopher (Thomomys talpoides) control of alpine plant community structure. Arct Antarct Alp Res 37:585–590

    Article  Google Scholar 

  • Simkin SM, Michener WK, Wyatt R (2001) Plant response following soil disturbance in a longleaf pine ecosystem. J Torrey Bot Soc 128:208–218

    Article  Google Scholar 

  • Simkin SM, Michener WK, Wyatt R (2004) Mound microclimate, nutrients and seedling survival. Am Midl Nat 152:12–24

    Article  Google Scholar 

  • Spencer SR, Cameron GN, Eshelman BD, Cooper LC, Williams LR (1985) Influence of pocket gopher mounds on a Texas coastal prairie. Oecologia 66:111–115

    Article  Google Scholar 

  • St. John MG, Bellingham PJ, Walker LR, Orwin KH, Bonner KI, Dickie IA, Morse CW, Yeates GW, Wardle DA (2012) Loss of a dominant nitrogen-fixing shrub in primary succession: consequence for plant and below-ground communities. J Ecol 100:1074–1084

    Article  Google Scholar 

  • Susfalk RB, Johnson DW (2002) Ion exchange resin based soil solution lysimeters and snowmelt solution collectors. Commun Soil Sci Plant Anal 33:1261–1275

    Article  CAS  Google Scholar 

  • Swanson FJ, Major JJ (2005) Physical events, environments, and geological–ecological interactions at Mount St. Helens: March 1980–2004. Ecological responses to the 1980 eruption of Mount St. Helens, pp 27–44

  • Thornton IWB, Compton SG, Wilson CN (1996) The role of animals in the colonization of the Krakatau Islands by fig trees (Ficus species). J Biogeogr 23:577–592

    Article  Google Scholar 

  • Titus JH (2008) Nitrogen-fixers Alnus and Lupinus increase soil fertility but not invasion by late successional species in primary succession on Mount St. Helens. Plant Ecol 203:289–301

    Article  Google Scholar 

  • Titus JH, Bishop JG (2014) Propagule limitation and competition with nitrogen-fixers limit conifer colonization during primary succession. J Veg Sci 25:990–1003

    Article  Google Scholar 

  • Tummers B (2006) DataThief III, vol 2010

  • Villarreal D, Clark KL, Branch LC, Hierro JL, Machicote M (2008) Alteration of ecosystem structure by a burrowing herbivore, the plains vizcacha (Lagostomus maximus). J Mammal 89:700–711

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. BioScience 25:376–381

    Article  CAS  Google Scholar 

  • Walker LR, Chapin FS III (1987) Interactions among processes controlling successional change. Oikos 50:131–135

    Article  Google Scholar 

  • Walker LR, del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Williams LR, Cameron GN, Spencer SR, Eshelman BD, Gregory MJ (1986) Experimental analysis of the effects of pocket gopher mounds on Texas coastal prairie. J Mammal 67:672–679

    Article  Google Scholar 

  • Wunderle JM (1997) The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. For Ecol Manag 99:223–235

    Article  Google Scholar 

  • Yang S, Jongejans E, Yang S, Bishop JG (2011) The effect of consumers and mutualists of Vaccinium membranaceum at Mount St. Helens: dependence on successional context. PLoS One 6:e26094

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zaitlin B, Hayashi M (2012) Interactions between soil biota and the effects on geomorphological features. Geomorphology 157–158:142–152

    Article  Google Scholar 

  • Zehetner F (2010) Does organic carbon sequestration in volcanic soils offset volcanic CO2 emissions? Quat Sci Rev 29:1313–1316

    Article  Google Scholar 

  • Zinnel KC, Tester JR (1990) Effects of plains pocket gophers on root biomass and soil nitrogen. In: Anonymous (ed) Proceedings of the twelfth North American prairie conference, University of Northern Iowa. Cedar Falls, pp 43–46

  • Zobel DB, Antos JA (1997) A decade of recovery of understory vegetation buried by volcanic tephra from Mount St. Helens. Ecol Monogr 67:317–344

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful for assistance and encouragement of M.K. Birchfield, M. Bosyj, C. Che-Castaldo, J. Csoka, P. Jensen, A. Kroon, J. Pitkin, D. Roberts, L. Shepard, A. Taras, E. Thomas, and M. Warman. The manuscript was greatly improved by the comments of anonymous reviewers. This work was supported by a grant to JGB from the National Science Foundation (DEB-0614538) and awards to RPY from the Washington State University Robert Lane Fellowship, the Society for Northwest Vertebrate Biology and National Science Foundation’s Partners in Discovery GK-12 program (Grant #07-42561).

Author information

Author notes

  1. Raymond P. Yurkewycz

    Present address: Mount St. Helens Institute, 42218 NE Yale Bridge Rd, Amboy, WA, 98601, USA

Authors and Affiliations

  1. School of the Environment, Washington State University, Vancouver, 14204 NE Salmon Creek Avenue, Vancouver, WA, 98686, USA

    Raymond P. Yurkewycz & John A. Harrison

  2. School of Biological Sciences, Washington State University, Vancouver, 14204 NE Salmon Creek Avenue, Vancouver, WA, 98686, USA

    John G. Bishop

  3. US Forest Service Pacific Northwest Research Station, Mount St. Helens National Volcanic Monument, 42218 NE Yale Bridge Rd, Amboy, WA, 98601, USA

    Charles M. Crisafulli

  4. Department of Biology, Brigham Young University, 151 WIDB, Provo, UT, 84602, USA

    Richard A. Gill

Authors
  1. Raymond P. Yurkewycz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John G. Bishop
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Charles M. Crisafulli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John A. Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Richard A. Gill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John G. Bishop.

Additional information

Communicated by Tim Seastedt.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yurkewycz, R.P., Bishop, J.G., Crisafulli, C.M. et al. Gopher mounds decrease nutrient cycling rates and increase adjacent vegetation in volcanic primary succession. Oecologia 176, 1135–1150 (2014). https://doi.org/10.1007/s00442-014-3075-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3075-7

Keywords

Search

Navigation