Skip to main content
Log in

Human altered disturbance patterns and forest succession: impacts of competition and ungulate herbivory

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Human activities are altering patterns of ungulate herbivory and wildfire regimes globally with large potential impacts on plant community succession and ecosystem resilience. Aspen (Populus tremuloides) is a keystone species which co-exists with conifer species across temperate forests in North America. Aspen sucker regeneration which is the foundation of aspen–conifer forests succession is often a targeted food source by multiple ungulate species. Using a region-wide exclosure network across a broad gradient of aspen–conifer overstory abundance, we empirically tested the effects of ungulate herbivory and conifer competition (that increases with fire suppression), on the regeneration and recruitment of aspen forests over a 4-year period. The study results indicate that ungulate herbivory and increasing abundance of overstory conifers dramatically reduced aspen regeneration and recruitment success. The average height of aspen suckers exposed to ungulate herbivory was 72% shorter than aspen suckers in fenced plots and resulted in 24% less recruitment. There was a 9% decrease in aspen recruitment and 12% decrease in average aspen height with every 20% increase in overstory conifer density. Aspen suckers were most vulnerable to herbivory at 70 cm height, with the probability of herbivory decreasing under 50 cm or above 90 cm. Steep slope angles and higher winter precipitation increased aspen regeneration and recruitment success. Reduction in aspen recruitment in response to ungulate herbivory and competition by conifers may result in loss of biodiversity, altered forest function and loss of key ecosystem services because of the important role that aspen plays in facilitating forest succession and biodiversity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams MA (2013) Mega-fires, tipping points and ecosystem services: managing forests and woodlands in an uncertain future. For Ecol Manag 294:250–261

    Article  Google Scholar 

  • Augustine DJ, Derner JD (2014) Controls over the strength and timing of fire–grazer interactions in a semi-arid rangeland. J Appl Ecol 51:242–250

    Article  Google Scholar 

  • Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manag 62:1165–1183

    Article  Google Scholar 

  • Beck JL, Peek JM (2005) Diet composition, forage selection, and potential for forage competition among elk, deer, and livestock on aspen–sagebrush summer range. Rangel Ecol Manag 58:135–147

    Article  Google Scholar 

  • Berdanier AB, Klein JA (2011) Growing season length and soil moisture interactively constrain high elevation aboveground net primary production. Ecosystems 14:963–974

    Article  Google Scholar 

  • Binkley D (2008) Age distribution of aspen in Rocky Mountain National Park, USA. For Ecol Manag 255:797–802

    Article  Google Scholar 

  • Bork EW, Carlyle CN, Cahill JF, Haddow RE, Hudson RJ (2013) Disentangling herbivore impacts on Populus tremuloides: a comparison of native ungulates and cattle in Canada’s Aspen Parkland. Oecologia 173:895–904

    Article  PubMed  Google Scholar 

  • Bowman D, Balch JK, Artaxo P, Bond WJ, Carlson JM, Cochrane MA, D’Antonio CM, DeFries RS, Doyle JC, Harrison SP, Johnston FH, Keeley JE, Krawchuk MA, Kull CA, Marston JB, Moritz MA, Prentice IC, Roos CI, Scott AC, Swetnam TW, van der Werf GR, Pyne SJ (2009) Fire in the earth system. Science 324:481–484

    Article  CAS  PubMed  Google Scholar 

  • Buck JR, Clair SBS (2012) Aspen increase soil moisture, nutrients, organic matter and respiration in Rocky Mountain forest communities. PLoS One 7:e52369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buck JR, St Clair SB (2014) Stand composition, proximity to overstory trees and gradients of soil moisture influence patterns of subalpine fir seedling emergence and survival. Plant Soil 381:61–70

    Article  CAS  Google Scholar 

  • Calder WJ, St Clair SB (2012) Facilitation drives mortality patterns along succession gradients of aspen-conifer forests. Ecosphere 3:1–11

    Article  Google Scholar 

  • Calder WJ, Horn KJ, St Clair SB (2011) Conifer expansion reduces the competitive ability and herbivore defense of aspen by modifying light environment and soil chemistry. Tree Physiol 31:582–591

    Article  CAS  PubMed  Google Scholar 

  • Dormann CF, McPherson JM, Araújo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Daniel Kissling W (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30:609–628

    Article  Google Scholar 

  • Franklin J, Syphard AD, He HS, Mladenoff DJ (2005) Altered fire regimes affect landscape patterns of plant succession in the foothills and mountains of southern California. Ecosystems 8:885–898

    Article  Google Scholar 

  • Frey BR, Lieffers VJ, Landhausser SM, Comeau PG, Greenway KJ (2003) An analysis of sucker regeneration of trembling aspen. Can J For Res 33:1169–1179

    Article  Google Scholar 

  • Frey BR, Lieffers VJ, Hogg EH, Landhausser SM (2004) Predicting landscape patterns of aspen dieback: mechanisms and knowledge gaps. Can J For Res 34:1379–1390

    Article  Google Scholar 

  • Gallant AL, Hansen AJ, Councilman JS, Monte DK, Betz DW (2003) Vegetation dynamics under fire exclusion and logging in a Rocky Mountain watershed, 1856–1996. Ecol Appl 13:385–403

    Article  Google Scholar 

  • Gervasi V, Sand H, Zimmermann B, Mattisson J, Wabakken P, Linnell JD (2013) Decomposing risk: landscape structure and wolf behavior generate different predation patterns in two sympatric ungulates. Ecol Appl 23:1722–1734

    Article  PubMed  Google Scholar 

  • Goetz S, Mack M, Gurney K, Randerson J, Houghton R (2007) Ecosystem responses to recent climate change and fire disturbance at northern high latitudes: observations and model results contrasting northern Eurasia and North America. Environ Res Lett 2:045031

    Article  Google Scholar 

  • Group PC (2004) Oregon State University. PRISM Climate Data

  • Hanley TA (1982) The nutritional basis for food selection by ungulates. J Range Manag 35:146–151

    Article  Google Scholar 

  • Harding SA, Jarvie MM, Lindroth RL, Tsai C-J (2009) A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast-and slow-growing Populus hybrid clones. J Exp Bot 60:3443–3452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison XA, Donaldson L, Correa-Cano ME, Evans J, Fisher DN, Goodwin CE, Robinson BS, Hodgson DJ, Inger R (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6:e4794

    Article  PubMed  PubMed Central  Google Scholar 

  • Holeski LM, Vogelzang A, Stanosz G, Lindroth RL (2009) Incidence of Venturia shoot blight in aspen (Populus tremuloides Michx.) varies with tree chemistry and genotype. Biochem Syst Ecol 37:139–145

    Article  CAS  Google Scholar 

  • Hollenbeck JP, Ripple WJ (2007) Aspen and conifer heterogeneity effects on bird diversity in the northern Yellowstone ecosystem. West N Am Nat 67:92–101

    Article  Google Scholar 

  • Johnstone JF, Hollingsworth TN, Chapin FS, Mack MC (2010) Changes in fire regime break the legacy lock on successional trajectories in Alaskan boreal forest. Glob Change Biol 16:1281–1295

    Article  Google Scholar 

  • Kauffman MJ, Brodie JF, Jules ES (2010) Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally mediated trophic cascade. Ecology 91:2742–2755

    Article  PubMed  Google Scholar 

  • Kaye MW, Binkley D, Stohlgren TJ (2005) Effects of conifers and elk browsing on quaking aspen forests in the central Rocky Mountains, USA. Ecol Appl 15:1284–1295

    Article  Google Scholar 

  • Knowles J, Frederick C (2016) merTools: tools for analyzing mixed effect regression models (R package version 0.2. 1). See https://CRAN.R-project.org/package=merTools. Accessed 15 May 2018

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2015) lmerTest: tests in linear mixed effects models (R package version:2-0). http://CRAN.R-project.org/package=lmerTest. Accessed 15 May 2018

  • LaMalfa EM, Ryle R (2008) Differential snowpack accumulation and water dynamics in aspen and conifer communities: implications for water yield and ecosystem function. Ecosystems 11:569–581

    Article  Google Scholar 

  • Launchbaugh KL, Howery LD (2005) Understanding landscape use patterns of livestock as a consequence of foraging behavior. Rangel Ecol Manag 58:99–108

    Article  Google Scholar 

  • Lindroth RL, St Clair SB (2013) Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores. For Ecol Manag 299:14–21

    Article  Google Scholar 

  • Long RA, Bowyer RT, Porter WP, Mathewson P, Monteith KL, Kie JG (2014) Behavior and nutritional condition buffer a large-bodied endotherm against direct and indirect effects of climate. Ecol Monogr 84:513–532

    Article  Google Scholar 

  • Mauricio R, Rausher MD, Burdick DS (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78:1301–1311

    Article  Google Scholar 

  • Midoko-Iponga D, Krug CB, Milton SJ (2005) Competition and herbivory influence growth and survival of shrubs on old fields: implications for restoration of renosterveld shrubland. J Veg Sci 16:685–692

    Article  Google Scholar 

  • Myking T, Bøhler F, Austrheim G, Solberg EJ (2011) Life history strategies of aspen (Populus tremula L.) and browsing effects: a literature review. Forestry 84:61–71

    Article  Google Scholar 

  • Mysterud A, Austrheim G (2014) Lasting effects of snow accumulation on summer performance of large herbivores in alpine ecosystems may not last. J Anim Ecol 83:712–719

    Article  PubMed  Google Scholar 

  • NRCS National Water and Climate Center, home (2019) https://www.wcc.nrcs.usda.gov/snow/snow_map.html. Accessed 2.5.19

  • Painter LE, Beschta RL, Larsen EJ, Ripple WJ (2015) Recovering aspen follow changing elk dynamics in Yellowstone: evidence of a trophic cascade? Ecology 96:252–263

    Article  PubMed  Google Scholar 

  • Pollard J (1971) On distance estimators of density in randomly distributed forests. Biometrics 991–1002

  • RC Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, p 2016

    Google Scholar 

  • Rehfeldt GE, Ferguson DE, Crookston NL (2009) Aspen, climate, and sudden decline in western USA. For Ecol Manag 258:2353–2364

    Article  Google Scholar 

  • Rhodes AC, Clair SBS (2018) Measures of browse damage and indexes of ungulate abundance to quantify their impacts on aspen forest regeneration. Ecol Ind 89:648–655

    Article  Google Scholar 

  • Rhodes AC, Anderson V, St Clair SB (2017a) Ungulate herbivory alters leaf functional traits and recruitment of regenerating aspen. Tree Physiol 37:402–413

    CAS  PubMed  Google Scholar 

  • Rhodes AC, Wan HY, Clair SBS (2017b) Herbivory impacts of elk, deer and cattle on aspen forest recruitment along gradients of stand composition, topography and climate. For Ecol Manag 397:39–47

    Article  Google Scholar 

  • Rogers PC, Mittanck CM (2014) Herbivory strains resilience in drought-prone aspen landscapes of the western US. J Veg Sci 25:457–469

    Article  Google Scholar 

  • Romme WH, Turner MG, Wallace LL, Walker JS (1995) Aspen, elk, and fire in northern Yellowstone-National-Park. Ecology 76:2097–2106

    Article  Google Scholar 

  • Seager ST, Eisenberg C, St Clair SB (2013) Patterns and consequences of ungulate herbivory on aspen in western North America. For Ecol Manag 299:81–90

    Article  Google Scholar 

  • Smith AE, Smith FW (2005) Twenty-year change in aspen dominance in pure aspen and mixed aspen/conifer stands on the Uncompahgre Plateau, Colorado, USA. For Ecol Manag 213:338–348

    Article  Google Scholar 

  • Smith EA, O’Loughlin D, Buck JR, Clair SBS (2011) The influences of conifer succession, physiographic conditions and herbivory on quaking aspen regeneration after fire. For Ecol Manag 262:325–330

    Article  Google Scholar 

  • Smith DS, Fettig SM, Bowker MA (2016) Elevated Rocky Mountain elk numbers prevent positive effects of fire on quaking aspen (Populus tremuloides) recruitment. For Ecol Manag 362:46–54

    Article  Google Scholar 

  • Spear D, Chown SL (2009) Non-indigenous ungulates as a threat to biodiversity. J Zool 279:1–17

    Article  Google Scholar 

  • St Clair SB, Cavard X, Bergeron Y (2013) The role of facilitation and competition in the development and resilience of aspen forests. For Ecol Manag 299:91–99

    Article  Google Scholar 

  • Strand EK, Vierling LA, Bunting SC, Gessler PE (2009) Quantifying successional rates in western aspen woodlands: current conditions, future predictions. For Ecol Manag 257:1705–1715

    Article  Google Scholar 

  • Tilman D, Isbell F, Cowles JM (2014) Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45:471–493

    Article  Google Scholar 

  • Turner MG (2010) Disturbance and landscape dynamics in a changing world. Ecology 91:2833–2849

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wagner CEV, Finney MA, Heathcott M (2006) Historical fire cycles in the Canadian Rocky Mountain parks. For Sci 52:704–717

    Google Scholar 

  • Wan HY, Olson AC, Muncey KD, Clair SBS (2014a) Legacy effects of fire size and severity on forest regeneration, recruitment, and wildlife activity in aspen forests. For Ecol Manag 329:59–68

    Article  Google Scholar 

  • Wan HY, Rhodes AC, St Clair SB (2014b) Fire severity alters plant regeneration patterns and defense against herbivores in mixed aspen forests. Oikos 123:1479–1488

    Article  CAS  Google Scholar 

  • Weisberg PJ, Bugmann H (2003) Forest dynamics and ungulate herbivory: from leaf to landscape. For Ecol Manag 181:1–12

    Article  Google Scholar 

  • Westerling AL (2016) Increasing western US forest wildfire activity: sensitivity to changes in the timing of spring. Philos Trans R Soc B Biol Sci 371:20150178

    Article  Google Scholar 

  • Wood S, Scheipl F (2014) gamm4: generalized additive mixed models using mgcv and lme4. R package version 0.2-3

  • Wooley SC, Walker S, Vernon J, Lindroth RL (2008) Aspen decline, aspen chemistry, and elk herbivory: are they linked? Aspen chemical ecology can inform the discussion of aspen decline in the West. Rangelands 30:17–21

    Article  Google Scholar 

  • Worrall JJ, Hogg EH, Rehfeldt GE, Hamann A, Michaelian M, Gray L (2012) Recent mortality episodes of Populus tremuloides and climate in North America. Phytopathology 102:137

    Google Scholar 

  • Worrall JJ, Rehfeldt GE, Hamann A, Hogg EH, Marchetti SB, Michaelian M, Gray LK (2013) Recent declines of Populus tremuloides in North America linked to climate. For Ecol Manag 299:35–51

    Article  Google Scholar 

  • Worrall JJ, Keck AG, Marchetti SB (2015) Populus tremuloides stands continue to deteriorate after drought-incited sudden aspen decline. Can J For Res 45:1768–1774

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge the important contributions of Justin Taylor, Rebecca Lee, and Ho Yi Wan for assistance in data collection. We are grateful for the assistance of the Fishlake, Dixie and Manti-Lasal National Forests for their assistance in establishing the exclosure networks.

Funding

Funding for this study was provided by the Utah Division of Natural Resources (2012).

Author information

Authors and Affiliations

Authors

Contributions

SS conceived the ideas and SS and AR set up the experimental design, AR and JM collected the data, JM analyzed the data, JM led the writing of the manuscript with the assistance of both SS and AR.

Corresponding author

Correspondence to Samuel B. St. Clair.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by Amy Austin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maxwell, J.D., Rhodes, A.C. & St. Clair, S.B. Human altered disturbance patterns and forest succession: impacts of competition and ungulate herbivory. Oecologia 189, 1061–1070 (2019). https://doi.org/10.1007/s00442-019-04370-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04370-8

Keywords

Navigation