Belowground effects of deer in a temperate forest are time-dependent

https://doi.org/10.1016/j.foreco.2021.119228Get rights and content

Highlights

  • Long-term deer presence increased soil compaction and decreased phosphorus.

  • Long-term deer presence correlated with changes in soil prokaryotic community.

  • Deer removal had no short-term effects on soil properties.

  • Deer exclusion significantly reduced soil compaction after twenty years.

  • Revealing deer belowground effects in temperate forests requires long-term studies.

Abstract

The past century witnessed a dramatic increase in deer abundance in North America, Western Europe, and Japan, that triggered profound changes in the vegetation structure of temperate forests. Considering the effects large herbivores can have on soil properties and organisms, it is likely that such increased deer abundance will have consequences belowground. Current studies in temperate forests, however, found inconsistent results regarding the effect of deer on soils within, and across, ecosystems. These inconsistencies may be the result of a time-dependent response of the soil to deer presence. Short-term belowground modifications may reflect the direct interactions of deer on soil (i.e. trampling and waste deposition), while long-term belowground modifications may reflect both direct and indirect effects of deer on soil (e.g. through vegetation shifts). To test these ideas, we measured the effects of deer on soil properties and prokaryotic communities in the temperate forests of Haida Gwaii, Canada. We compared three complementary systems varying in duration of deer presence or exclusion, so as to be able to assess the short- (before and after a deer cull), intermediate- (inside vs. outside deer exclosures) and long- (comparing islands with and without deer) term effects of deer, respectively. We found no change in soil physical and chemical properties and in prokaryotic community structure after one year of deer removal. Twenty years of deer exclusion significantly reduced soil compaction but had no effect on soil prokaryotic community structure. Over 70 years of deer presence significantly correlated with: increased soil compaction, reduced total soil phosphorus content and soil prokaryotic diversity, and modified soil prokaryotic community structure and composition. Such effects of deer on the soil may have consequences for nutrient cycling. Revealing the belowground effects of deer in temperate forests, therefore, requires long-term studies, longer than most of those currently available in the literature.

Introduction

Large herbivores can influence belowground soil properties and communities directly through trampling and waste deposition, and indirectly through plant removal (Bardgett and Wardle, 2003, Schrama et al., 2013). To date, interactions between large herbivores and soil have been highlighted for a broad range of ecosystems and herbivores, from sheep-grazed pastures to moose-browsed old-growth boreal forests (Andriuzzi and Wall, 2017, Bardgett et al., 1997, Pastor et al., 1993). The effects of large herbivores on soils depend on ecosystem characteristics such as ecosystem type, climate, herbivore size, and soil properties (Andriuzzi and Wall, 2017, Bardgett and Wardle, 2003, Schrama et al., 2013). Soil properties and organisms are central to carbon and nutrient recycling (Wardle et al. 2004). As a result, belowground modifications caused by large herbivores can have major feedbacks on ecosystem functioning and on aboveground organisms through the acceleration or the deceleration of these biogeochemical cycles (Bardgett and Wardle, 2003, Wardle et al., 2004).

The past century witnessed a dramatic increase in deer abundance at continental scales in temperate forests of North America, Western Europe, and Japan (Côté et al., 2004, Fuller and Gill, 2001, Takatsuki, 2009). This massive increase has triggered major changes in the structure of temperate forests including the prevention of tree regeneration, a reduction in understory biomass, the modification of understory plant composition, and negative reverberating effects on other trophic layers such as birds and insects [see among others (Cardinal et al., 2012, Côté et al., 2004, Martin et al., 2010, Nuttle et al., 2011, Ramirez et al., 2018, Takada et al., 2008)]. Considering the interactions between large herbivores and soil described above, increased deer abundance in temperate forests may have significant consequences belowground. In forest ecosystems, the effects of large herbivores on soil have been predicted to be driven mainly by the reduction of litter quantity and quality. Such reduction is a consequence of the promotion of less palatable plant species due to selective browsing, that surmounts the effects of nutrient input from dung and urine deposition (Bardgett and Wardle, 2003, Chollet et al., 2020). As a result, a negative effect of deer on nutrient availability and biological activity is expected in forest ecosystems (Bardgett and Wardle, 2003). Current studies on the belowground effects of deer in temperate forests, however, found inconsistent results within, and across, systems (Bardgett et al., 1998, Bardgett and Wardle, 2003, Harrison and Bardgett, 2008). For example, the effects of deer on soil properties were found to be significant (e.g. Bressette et al., 2012, Gass and Binkley, 2011, Niwa et al., 2011), neutral (Relva et al. 2014), or idiosyncratic (Wardle et al., 2001; Harrison and Bardgett, 2004). In light of the profound aboveground modification of forest ecosystems by persistent abundant deer populations, understanding the interactions between deer and soil, and being able to predict their effects on edaphic properties and processes, is a forest management and conservation necessity. It is also essential for a comprehensive understanding of ecological processes in temperate forests.

We hypothesised that some of the discrepancies currently observed across and within belowground studies in temperate forests may result from the approaches and methodologies used. Particularly, the length of the study could act as a key confounding factor. To date, the method of choice to study deer effects on ecosystems has been by excluding deer from fenced areas known as exclosures. The comparison of ecosystem characteristics inside and outside of exclosures over time provides information on the ecosystem’s resilience following deer exclusion and, therefore, on the effects deer have exerted on the ecosystem. The duration of exclusion varies widely across studies. Exclusion usually lasts in the range of a decade (Andriuzzi and Wall, 2017); however, the mechanisms through which deer interact with soil are not all operating at the same temporal and spatial scale. Changes in the plant community could take decades and operate at the ecosystem scale, while the deposition of dung or urine, or its cessation through deer exclusion or severe cull, are local and near instantaneous processes. Time since deer exclusion must, therefore, play a key role in the patterns revealed by exclosure studies.

To test the hypothesis of the importance of study length, we compared the effect of different deer browsing histories on soil ecosystem properties and soil prokaryotic communities in a temperate forest. We used three complementary systems varying in length of deer presence or exclusion to assess the short-, intermediate- and long-term effects of deer. We conducted our study on the Canadian archipelago of Haida Gwaii (B.C., Canada), where Sitka black-tailed deer (Odocoileus hemionus sitkensis), introduced over 100 years ago, inhabit all but a few islands. We first followed the short-term effects of deer in response to a recent deer cull on Ramsay Island (Haida Gwaii). In this system, we assessed the rapid (one month after the cull) to short-term (one year after the cull) responses of the vegetation and soil to deer removal. We then studied a set of 20-year old deer exclosures distributed on Graham Island, the largest of the archipelago’s islands, where deer have been present since the late 1800s to early 1900s. This deer exclosure system enabled us to compare the medium-term (20 years) effects of total deer exclusion to the effects of a century-long presence of an abundant deer population. Finally, we took advantage of a unique situation on Haida Gwaii where deer colonisation of the archipelago resulted in the presence, in close proximity, of a small number of islands that had never been colonised by deer, and islands that had been colonised for more than 70 years at the time of this study (Vila et al., 2004). In this third system, the comparison of the deer-colonised islands to the un-colonised islands allowed us to study the long-term effects of deer colonisation on the soil.

We predicted that the short-term modifications of the belowground subsystem, investigated using our recent deer cull study system, would be driven by the direct interaction of deer with edaphic properties through trampling and/or waste deposition. The local-scale nature of waste deposition by deer and the soil-type specific response to compaction may, therefore, explain part of the idiosyncrasies observed within and among short studies (Murray et al., 2013, Schrama et al., 2013). Conversely, the indirect effects of large herbivores via changes in the vegetation composition and structure should be longer-term processes acting at the ecosystem scale. Revealing their consequences belowground will, therefore, require lengthier studies (Bardgett et al., 2005). In this respect, we predicted that such indirect effects of deer would drive the differences belowground in our deer exclusion study system and in our deer colonisation study system.

Section snippets

Study sites and sampling

Haida Gwaii is an archipelago located off the west coast of British Columbia, Canada (latitude 53.255, longitude −132.087). The climate is cool, temperate and oceanic. Mean annual temperature and precipitation are 7.6 °C and 1349 mm, respectively (Meidenger and Pojar, 1991). At low altitude, Haida Gwaii is covered with a coastal temperate rainforest that is dominated by western hemlock (Tsuga heterophylla), western redcedar (Thuja plicata), and Sitka spruce (Picea sitchensis). Soil bedrock

Deer affected understory vegetation in a consistent way across the three study systems

In the recent deer cull system, the first axis of the PCA discriminated vegetation from the plots on the islands that have or had deer present (‘present’ and ‘culled’ treatments) from plots on islands without deer (‘absent’ treatment) (Fig. 1A). The second PCA axis discriminated between years of sampling (Fig. 1A). Interaction between treatments and year of sampling was significant for the vascular plant and bryophyte diversities, and the bryophyte and forb cover (Table A2 and Fig. A2). Among

Discussion

Current studies investigating the belowground effects of deer in temperate forests have found inconsistent results within, and across, systems (Bardgett et al., 1998, Bardgett and Wardle, 2003, Harrison and Bardgett, 2008). In this study, we compared three different approaches varying in length of deer presence and exclusion to investigate the effects of deer belowground. While the effects of deer on the vegetation were consistent among the three study systems, we found that the response of the

Conclusions

We found that aboveground effects of deer were consistent among the three study systems, reflecting a temporal shift in the vegetation in response to deer presence that was consistent with plant growth patterns and requirements. The effects of deer on soil properties and organisms were time-dependent. The belowground response to deer was driven by waste deposition and trampling in the short-term and by trampling and vegetation shift in the long-term. Long-term changes in soil compaction and pH

CRediT authorship contribution statement

Morgane Maillard: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review & editing. Jean-Louis Martin: Conceptualization, Investigation, Project administration, Resources, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing. Simon Chollet: Conceptualization, Data curation, Formal analysis, Investigation, Validation, Visualization, Writing - original draft,

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This research was financially supported by the France Canada Research Fund (FCRF), the “The Llgaay gwii sdiihlda: Restoring Balance project” from Parks Canada, the Mitacs Globalink Research Award, NSERC Discovery Grant Funding, UBC Forestry IMAJO Award and the funding ‘Equipe de Recherche Junior’ from the LabEx CeMEB. It also received in kind and funds from RGIS, and critical local supports including help from the Laskeek Bay Conservation Society. We would like to thank Maria Continentino,

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