Patterns and consequences of ungulate herbivory on aspen in western North America
Graphical abstract
Highlights
► Aspen ecosystems have a bottom–up structure of soil, light, and resources. ► Ungulate browsing impacts soils, plant community, and stand demography. ► Aspen uses chemical defense and tolerance as strategies to cope with herbivory. ► Environmental modifiers of herbivory include climate change, fire, predators, and humans. ► Fire, ungulate density, and land management can modify aspen ecosystem resilience.
Introduction
Alterations to historic patterns of quaking aspen (Populus tremuloides) distribution, range, regeneration, and recruitment have been attributed to human-caused changes. Direct and indirect human impacts to aspen have occurred via manipulation of game and predator populations, livestock grazing, timber harvest, fire suppression, and climate change (Leopold et al., 1947, Hessl, 2002, Binkley et al., 2003, White et al., 2003).
Ungulate herbivory can be a key limiting factor in aspen recruitment into the forest canopy and persistence at the local scale (Baker et al., 1997, Suzuki et al., 1999, Kay and Bartos, 2000, Bailey and Witham, 2002). Intense, chronic browsing can degrade aspen community structure and diversity and simplify food webs (Leopold, 1943, White et al., 2003, Hebblewhite et al., 2005, Eisenberg, 2012), thereby reducing aspen ecosystem resilience, or capacity to recover quickly from perturbation or disturbance (Holling, 1973). Other environmental factors (e.g., drought and pathogens) can exacerbate the impact of ungulate herbivory in aspen forests (Worrall et al., 2008).
Bottom–up and top–down forces shape ecological communities (Schmitz et al., 2000). Bottom–up effects are defined as energy flow through a food web that stimulates or reduces vegetation growth (Borer et al., 2005). Top–down effects are those directly and indirectly related to predation. Here we provide a more integrated view of how bottom–up and top–down forces function in aspen forests, within the context of ungulate herbivory in western North America. We present a conceptual model (Fig. 1) to help synthesize these forces and their interactions. We conclude by offering management suggestions aimed at increasing resilience in aspen forest communities experiencing heavy browse pressure.
Section snippets
Bottom–up structuring in aspen ecosystems
Aspen is shade intolerant (Kobe and Coates, 1997), drought sensitive (Hogg et al., 2008), and has relatively high nutrient demand (Jug et al., 1999). As a result, aspen tends to favor siltier soils with greater soil moisture and nutrients (Hogg et al., 2008, Woldeselassie et al., 2012) and is affected differently by topography along its extensive elevational and latitudinal gradient (Little, 1971, Chen et al., 2002). Aspen stands typically allow greater understory light penetration (Powell and
Herbivore impacts on physical and chemical soil properties
Ungulates can alter organic inputs and change soil physical and chemical properties, affecting the nutrient cycling and net primary production in ecosystems (Binkley et al., 2003, Hobbs, 1996, Pastor et al., 1988). Low levels of herbivory may enhance nutrient cycling and plant growth through the deposit of dung and urine, although this benefit depends on the ungulates staying in the systems where biomass is consumed (Dyer et al., 1993, De Mazancourt et al., 1998). In Rocky Mountain National
Aspen defense strategies
Chemical defense is a primary strategy employed by aspen to control herbivory (Lindroth and St. Clair, 2013). Aspen allocate significant resources to the production of two phenolic-based defense compounds (phenolic glycosides and condensed tannins), which can make up more than 25% of the dry leaf weight of younger ramets that are more susceptible to browse pressure. Tannins have been shown to interfere with food digestibility in deer and livestock (Hagerman et al., 1992). While it is well known
Climate influences on ungulate herbivory in aspen forests
Drought and heat-induced aspen forest dieback (Allen et al., 2010, Worrall et al., 2010, Hanna and Kulakowski, 2012) can exacerbate patterns and impacts of ungulate herbivory. In the Rocky Mountains, monotypic, mature aspen stands are more susceptible to drought mortality, and thus stands with chronic herbivory of sprouts and young ramets, are more likely to experience stand collapse (Worrall et al., 2008, Zegler et al., 2012).
Brodie and others (2012) found that reduced snow pack that results
Exclosures, refugia, and jackstraw
Ungulate exclosures have been used extensively to test for herbivory impacts on aspen (Grimm, 1939, Costelo and Turner, 1941, Leopold, 1943, Binkley et al., 2006). While there is considerable debate over herbivory being the primary cause of the aspen decline (Romme et al., 1995), exclosure studies have shown that at the local scale, removal of ungulates allows aspen recruitment to occur (Fig. 4). This has been shown on diverse landscapes across western North America (Leopold, 1943, Mueggler and
Conclusion
While ungulate impacts on aspen ecosystems across western North America are not uniform, chronic and severe herbivory degrades the structure and function of aspen forests (White et al., 1998). The negative effects of ungulate herbivory can interact with environmental factors, decreasing aspen resilience to the point of stand senescence or collapse (Ripple et al., 2001, Worrall et al., 2010). Recent aspen dieback across western North America (Hanna and Kulakowski, 2012) creates an urgent need to
Acknowledgements
We thank the High Lonesome Ranch of DeBeque, Colorado for their support of the presentation of this paper at the Resilience in Quaking Aspen: Restoring Ecosystem Process Through Applied Science symposium. Sponsors of the symposium were: American Forest Foundation, Brigham Young University, High Lonesome Ranch, USDI Bureau of Land Management, Utah State University, and Western Aspen Alliance. We also thank Lauren Maglaska for technical assistance with ArcGIS and Bob Cambpell and Dale Bartos for
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