Forest Ecology and Management

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1 Forest Ecology and Management xxx (2013) xxx xxx Contents lists available at SciVerse ScienceDirect Forest Ecology and Management journal homepage: Patterns and consequences of ungulate herbivory on aspen in western North America S Trent Seager a,, Cristina Eisenberg a, Samuel B. St. Clair b a Department of Forest Ecosystems and Society, Oregon State University, Corvallis, OR, USA b Department of Plant and Wildlife Sciences, Brigham Young University, Provo, UT, USA article info abstract Article history: Available online xxxx Keywords: Ungulate herbivory Aspen ecosystems Populus tremuloides Elk and deer densities Environmental modifications Quaking aspen (Populus tremuloides) forests develop complex, multi-story structure and speciose plant communities, which provide habitat for ungulates and diverse wildlife species. Successfully recruiting aspen sprouts and seedlings provide important sources of structural, functional and genetic diversity vital to resilient aspen forests. Chronic ungulate browsing of regenerating aspen can degrade aspen community structure and diversity. This simplifies food webs and can have negative implications for ecosystem resilience. This paper explores how patterns of ungulate herbivory in aspen forests are influenced by and affect bottom up and top down forces in aspen ecosystems. We outline management strategies aimed at decreasing ungulate and livestock impacts on aspen and increasing sprout survival and recruitment. The body of aspen research indicates that herbivory is more heterogeneous in areas that contain human hunters, predators, or fire on the landscape. The complexities of ungulate herbivory and fire on aspen ecosystems, especially in relation to scale, are imperfectly understood. Wildlife agencies responsible for elk (Cervus elaphus) and deer (Odocoileus spp.) populations should consider management strategies that use ungulate herbivory impacts on ecosystems such as aspen as indicators of sustainable herd densities. To increase aspen resilience in the face of current and future environmental change, we recommend a multi-faceted approach that involves enhancing bottom up forces while decreasing top down impacts from ungulates. Ó 2013 Elsevier B.V. All rights reserved. 1. 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 Corresponding author. Address: 321 Richardson Hall, Corvallis, OR 97331, USA. Tel.: address: trent.seager@oregonstate.edu (S Trent Seager). 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. 2. 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 /$ - see front matter Ó 2013 Elsevier B.V. All rights reserved.

2 2 S Trent Seager et al. / Forest Ecology and Management xxx (2013) xxx xxx 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 Park (RMNP), Binkley and others (2003) found no difference in soil nitrogen or carbon between aspen stands grazed by elk and areas where they were experimentally excluded over a 35-year period. Elk movements in RMNP create a transfer and loss of nutrients from the system, which can reduce the growth potential of aspen and willow (Salix spp.) (Schoenecker et al., 2004) Herbivory impacts on understory plant community composition Fig. 1. Conceptual model of drivers and dynamics in aspen ecosystems within the context of ungulate herbivory. Aspen ecosystems have bottom up structuring and top down control, which can be influenced by environmental modifiers (solid lines show direct effect; dashed lines show potential and indirect effects). Bottom up structuring comes from soil properties, influenced by climate, fire, and human impact such as timber harvest. Top down control occurs from ungulate herbivory of aspen via direct predation and potential impact on bottom up forces. Potential herbivory modifiers include aspen defense strategies, trophic cascades, and environmental modifiers (climate change, fire, and human impacts). penetration (Powell and Bork, 2006) and have higher soil resource availability than adjacent conifer stands (Buck and St. Clair, 2012). This contributes to high plant biodiversity and productivity in aspen understories (Kuhn et al., 2011). Tall shrubs and young aspen ramets form a midstory canopy structure that adds to the structural diversity of aspen stands (Mueggler, 1988; Eisenberg, 2012). The structural diversity and productivity in aspen forests creates habitat for a wide diversity of wildlife (Reynolds, 1969; Debyle, 1985; Turchi et al., 1995; Hollenbeck and Ripple, 2007; McCullough et al., 2012). Aspen understories are a rich in small mammal diversity (Oaten and Larsen, 2008) and provide important habitat for elk (Cervus elaphus) and deer (Odocoileus spp.) (Preble, 1911; Murie, ; Beck and Peek, 2005). Aspen s predisposition to heart-rot creates excellent habitat for primary and secondary cavity nesting species, including birds, squirrels, and mice (Flack, 1976; Martin and Eadie, 1999; Griffis-Kyle and Beier, 2003; Martin et al., 2004). Additionally, aspen forests host dynamic food webs that support a diverse guild of predators including, goshawks (Accipiter gentilis), coyotes (Canis latrans), bobcats (Lynx rufus), bears (Ursus spp.) and wolves (Canis lupus) (Debyle, 1985; Fisher and Wilkinson, 2005). 3. Top down control in aspen ecosystems 3.1. Herbivore impacts on physical and chemical soil properties Ungulate browse preference based on plant palatability and nutritional quality can shift understory vegetation composition and decrease species richness (Augustine and McNaughton, 1998). In Utah, Kay and Bartos (2000) found that mule deer (Odocoileus hemionus) browsing increased grasses, while decreasing shrub and forb height. This effect was compounded when livestock (primarily cattle) grazing coincided with deer herbivory. Moderate deer browsing can increase forest understory diversity, especially when browsing interacts with other disturbance processes, such as gaps in the overstory and fire in the understory (Royo et al., 2010). However, high elk and deer densities (>4 /km 2 ) and chronic herbivory suppress shrub density and height, reducing understory and midstory habitat important to many wildlife species (White et al., 1998; Kay, 2001a). Chronic herbivory from wild ungulates and domestic livestock can decrease native plant species, and increase the potential for plant invasion (Vavra et al., 2007). This can lead to opportunistic invasion of the aspen understory by non-native plants (primarily grasses) (Debyle, 1985). In elk winter range in Yellowstone National Park (YNP), Kay (2001b) comparing plant species composition inside and outside long-term exclosures, found that elk preferentially removed shrubs, enabling non-native grasses to dominate. Selective browsing on native flowering plants can also alter the balance between native and invaded plant communities through indirect effects on pollinator communities (Chong et al., 2001) Herbivory impacts on aspen stand demography and composition Long-term or heavy ungulate browsing can alter aspen demography and composition. Aspen have higher nutrient value than slower-growing trees, and thus are more appealing to ungulates as a food source (Cebrian and Duarte, 1994; Cook, 2002). Herbivory in aspen by wild ungulates and domestic livestock suppresses overstory tree recruitment, which alters the overstory structure and composition over time (Smith et al., 1972; Fitzgerald et al., 1986; McLaren and Peterson, 1994; Rooney and Waller, 2003; Wisdom et al., 2006; Didion et al., 2009). Leopold (1943) reported that irruptive deer populations heavily browsed aspen sprouts and removed cohorts which degraded aspen forests. However, the impact of ungulates on tree persistence is dependent upon context and scale. For example, Suzuki and others (1999) found that browsing by large ungulates impacted aspen abundance and demography at a local scale, but was not leading to the decline of aspen on landscape scales in the Colorado Front Range. A review of European aspen (Populus tremula L.) in Norway found similar conclusions (Myking et al., 2011). Chronic and long-term herbivory can have a negative effect on aspen stem recruitment, creating what is known as missing age classes (Bartos et al., 1994; Ripple and Larsen, 2000) (Fig. 2). This diminishes stand structural diversity, resulting in a decrease in wildlife abundance and diversity in over-browsed stands (Yahner, 1987; see Section 3.4). Missing age classes may also diminish clone fitness and resilience (Smith et al., 2011a). Studies of aspen dieback across in southwestern Colorado found that younger cohorts of aspen were more likely to survive drought and associated stressors, allowing them to persist in areas where older aspen stands

3 S Trent Seager et al. / Forest Ecology and Management xxx (2013) xxx xxx 3 Fig. 2. Aspen stand in St. Mary Valley in Glacier National Park showing chronic and heavy herbivory on the mature aspen stem boles and the lack of sprouts. Photo: Cristina Eisenberg. tend to die off (Worrall et al., 2008, 2010). As a result, when excessive browsing eliminates younger aspen age cohorts, stand resilience can be compromised. Elk and moose (Alces alces) chew or damage the bark and cambium of mature aspen stems (Fig. 2), especially when aspen understory vegetation and sprouts are unavailable because of chronic herbivory or winter conditions (DeByle, 1985; Miquelle and van Ballenberghe, 1989). Bark damage can predispose aspen stems to mortality via pathogenic fungi (Hart and Hart, 2001; White et al., 2003) or may kill aspen directly by damaging the peripheral vascular tissue (Packard, 1942). Aspen stands have been shown to successfully recruit during stochastic events that dramatically decrease ungulate populations or herbivory pressure (Kay and Bartos, 2000; Larsen and Ripple, 2003). However, aspen is a relatively short-lived species, so persistent herbivory pressure can lead to recruitment failure and stand senescence (Hessl, 2002). Accurate spatial data on ungulate densities on summer and winter range can provide important insights on herbivory patterns in aspen forests (Kashian et al., 2007). We were unable to find consistent or accurate ungulate density data in the Western US due to differences in herd count and population estimation methods among states and wildlife agencies (Idaho Department of Fish and Game, 1999, 2008; Utah Department of Wildlife Resources, 2010). Colorado Parks and Wildlife (2012) offers perhaps the most detailed and comprehensive data on elk herd density, including a breakdown on summer and winter range by area. A survey of North American research on differing elk densities and their effect on aspen sprout growth show a clear trend in which higher elk densities (4 10 elk/km 2 ) suppressed aspen recruitment into the overstory (Table 1). This is consistent with several studies showing that high elk density and associated chronic browsing limits aspen ramets from recruiting into the overstory (Hessl and Graumlich, 2002; White et al., 2003). While moose browse aspen sprouts and the bark of mature trees (Miquelle and van Ballenberghe, 1989) this impact tends to be localized as moose prefer other browse, such as willow, occur at low density ( /km 2 ), and are more evenly distributed on the landscape in relation to elk (Gasaway et al., 1992; Boertje et al., 1996; Dungan et al., 2010). In 1947, Leopold and his co-authors mapped ungulate problem areas (Fig. 3) and provided case histories. Recent aspen herbivory hotspots published in the scientific literature (Table 2) occur in the same historic deer and elk problem areas identified by Leopold and authors over a half century ago (Fig. 3, #1 9). This shows that many of the areas recently identified as lacking aspen recruitment were mapped as deer and elk problem areas in Based on current science, we would expect ungulate irruptions (defined as an exponential increase in population) from the first half of the century to create missing age classes in aspen ecosystems (White et al., 1998; Ripple and Larsen, 2000). Herbivory pressure has remained high and even increased with game management policies in many areas of western North America since the Leopold study (Fig. 3), suggesting we should continue to expect missing age classes and heavy browsing impacts in western aspen forests Herbivory effects on bird and insect communities Ungulate herbivory can modify aspen understories. Disturbance created by light to moderate browsing in areas with a high aspen Table 1 Elk densities and aspen recruitment (showing general trends, see specific studies for details). Study Study site Elk density or population Method of measurement Winter or summer range? Multiple stands with aspen recruitment? White et al. (2003) Ya Ha Tinda >10 /km 2 Pellet transects Winter No Jasper NP >5 /km 2 Pellet transects Winter No Banff NP Town >5 /km 2 Pellet transects Winter No Banff NP Mid 2 4 /km 2 Pellet transects Winter Yes (some) Bow valley 2 4 /km 2 Pellet transects Winter Yes (some) North Saskatchewan 2 4 /km 2 Pellet transects Winter Yes (some) Eastslopes-South <2 /km 2 Pellet transects Winter Yes Jasper-Willow Creek <1 /km 2 Pellet transects Winter Yes Wateron Lakes NP <1 /km 2 Pellet transects Winter Yes Eisenberg (2012) Waterton Lakes NP 24 /km 2 Pellet transects, aerial park Winter No counts Glacier NP St. Mary 21 /km 2 Pellet transects Winter No North Fork 8 9 /km 2 Pellet transects Winter No, unless fire and wolves Kimble et al. (2011) Gallatin NF GYNP Tom Miner 5 8 /km 2 State/federal census Winter No East River 2 5 /km 2 State/federal census Winter No West River 2 3 /km 2 State/federal census Winter No

4 4 S Trent Seager et al. / Forest Ecology and Management xxx (2013) xxx xxx Fig. 3. Comparison of ungulate problem areas identified by Leopold and others (1947) (noted by circular black dots ) to recent research of chronic ungulate herbivory on aspen (noted by boxed numbers 1 9). Numbers refer to specific studies. See Table 2 for study details and comparison. Map based on Leopold and others (1947). sprout density can increase understory diversity and heterogeneity (Krzic et al., 2003; Royo et al., 2010), which can increases wildlife and insect diversity (Debyle, 1985; Bailey and Witham, 2002). High elk density and heavy browsing can remove shrubs, understory structure, and ground litter, all of which greatly decreases wildlife presence and diversity (Flack, 1976; Hebblewhite et al., 2005) and reduces the species richness of birds (Hobson and Bayne, 2000; Aitken and Martin, 2004; Martin et al., 2004; Hollenbeck and Ripple, 2008) and insects (Chong et al., 2001; Bailey and Witham, 2002; Allombert et al., 2005). 4. Aspen defense strategies Chemical defense is a primary strategy employed by aspen to control herbivory (Lindroth and St. Clair, this issue). Aspen allocate significant resources to the production of two phenolicbased 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 that phenolic glycosides deter insect herbivores (Hemming and Lindroth, 1995), much less is known about their role in controlling ungulate browsing. Young aspen suckers have 3 4 times more foliar phenolic glycosides then juvenile ramets that have escaped ungulate herbivory through vertical growth (Donaldson and Lindroth, 2007; Smith et al., 2011a). From an evolutionary perspective, this suggests that herbivory pressure has contributed to increased defense chemistry expression in young aspen stems that are prone to browsing. Wooley and others (2008) demonstrated that captive elk preferred aspen genets containing lower phenolic glycoside concentrations. This indicates that high foliar phenolic glycoside concentrations can deter ungulate herbivory. During periods of high browse pressure, chemical defenses may contribute to the persistence of undamaged genotypes (Lindroth, 2001). In RMNP, divergent findings of elk impacts on aspen recruitment (Baker et al., 1997; Kaye et al., 2003; Kashian et al., 2007) may be partially explained by differences in defense chemistry profiles. However, under chronic browse pressure even well-defended genotypes may not avoid browse damage (Hessl, 2002). Table 2 Comparison of Leopold and others (1947) ungulate problem areas to recent Aspen-Herbivory studies (see Fig. 3 for locations and map). State and problem area Leopold et al. (1947) Recent research Aspen-Herbivory findings Location Ungulate species Study citation Ungulate species 1. Arizona Woods Mt. Mule deer Fairweather et al. (2007) Elk a, Mule deer Chronic herbivory (elk), no recruitment outside exclosures Rolf (2001) Chronic herbivory (elk), no recruitment after 30% reduction Zegler et al. (2012) Chronic herbivory (elk), damage to stems and sprouts 2. California Lassen NF Mule deer Jones et al. (2005) Mule deer Chronic herbivory, low recruitment w/o fencing 3. Colorado Rocky Mt. NP Mule deer, elk Baker et al. (1997) Elk a, deer, moose Chronic herbivory, low recruitment outside exclosures Kaye et al. (2003) Patchy herbivory, recruitment in some stands White et al. (1998) Chronic herbivory, low recruitment outside exclosures 4. Montana Glacier NP Deer Eisenberg (2012) Elk a, deer, moose Chronic herbivory (elk), no recruitment w/o fire and wolves 5. Oregon John Day Mule deer, elk Swanson et al. (2010) Elk a, Mule deer Chronic herbivory, no recruitment w/o exclosures 6. Oregon Klamath Deschutes Co. Mule deer Seager (2010) Mule deer a, elk Chronic herbivory, no recruitment w/o barriers 7. Utah Wasatch Mts, Dixie Deer, elk Kay and Bartos (2000) Mule deer a, elk Chronic herbivory, little recruitment w/o exclosures Smith et al. (2011b) Little herbivory, recruitment after 31,000 ha fire 8. Wyoming Yellowstone NP Mule deer, elk Romme et al. (1995) Elk a, deer, moose Chronic herbivory, little recruitment w/o barriers Ripple et al. (2001) Chronic herbivory across time, no recruitment w/o wolves Kauffman et al. (2010) Chronic herbivory, little recruitment w/o exclosures Romme et al. (2011) Chronic herbivory, little recruitment w/o exclosures 9. Wyoming Black Hills White-tailed deer Kota and Bartos (2010) Elk a, deer Chronic herbivory, little recruitment w/o barriers Keyser et al. (2005) Heavy herbivory, recruitment may not occur w/o barrier Dominant herbivore. a

5 S Trent Seager et al. / Forest Ecology and Management xxx (2013) xxx xxx 5 Aspen demonstrate adaptive use of defense strategies. Genotypic variation in defense chemistry suggests that there are tradeoffs to investing heavily in defense chemistry. Tolerance (traits focused on compensating for damage) and escape through vertical growth are alternative strategies employed by aspen to effectively deal with ungulate herbivores. Environmental conditions have a large influence on the efficacy of these three defense strategies. Tolerance and escape are probably more effectively strategies when browse pressure is high. Studies have shown that light and nutrient availability influence aspen chemical defense production (Donaldson et al., 2006; Osier and Lindroth, 2006). Conifer expansion resulting in reduced light and soil resource availability increases aspen susceptibility to browsing by decreasing vertical growth rates and the production of phenolic glycosides (Calder et al., 2011). With constant spatial and temporal shifts in browse pressure, aspen chemical defenses play an important role in aspen resilience against browsing (Lindroth and St. Clair, this issue), especially in areas where other management options for altering herbivory pressure are limited. 5. Environmental modifications of herbivory 5.1. 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 from warmer winters allowed elk to access aspen stems throughout the winter months, which increased bark damage and browsing intensity. Martin and Maron (2012) found that excluding elk alone allowed aspen and associated vegetation to increase during low snow years. The increase in drought and shifting precipitation patterns associated with global climate change highlights the importance of mitigating herbivory impacts in aspen ecosystems (Hogg et al., 2008; Rehfeldt et al., 2009; Worrall et al., 2010) Effects of fire on ungulate browsing in aspen Fire is a key factor in aspen ecology. Across diverse landscapes in western North America, fire kills mature aspen stems and stimulates vigorous root sprouting (Romme et al., 1995; Smith et al., 2011b). Where there is high ungulate activity, aspen abundance, fire size, and regeneration vigor all likely influence the ability of aspen to successfully regenerate (Smith et al., 2011b). Many studies on elk winter range have found that the increase in aspen sprouts post-fire attracts elk, resulting in little to no aspen recruitment (Romme et al., 1995, 2011; Baker et al., 1997; Barnett and Stohlgren, 2001; Kay, 2001b; Bailey and Witham, 2002; Hessl and Graumlich, 2002). Working in relatively small burned areas (200 ha), Bartos and others (1994) found that even though aspen stands produced high levels of aspen sprouts post-fire, elk herbivory continued to suppress sprouts from recruiting into the canopy 12 years later. However, in a large-scale (31,000 ha) fire complex in the Dixie National Forest in Utah, in an area with abundant elk and deer, Smith and others (2011b) found successful aspen regeneration. They hypothesized that high aspen suckering densities distributed over a larger areas saturated the browsing capacity of the deer and elk in this area. Fire severity can also influence aspen susceptibility to herbivory. High severity fire has been shown to stimulate aspen suckering, but reduces shrub and herbaceous cover, which may increase the focus of browsers on aspen (Bates et al., 2006). Elk herbivory was nearly three times greater in high versus low fire severity areas (Bailey and Witham, 2002). However, the effects of fire severity on aspen susceptibility to herbivory can be complex (Lindroth and St. Clair, this issue). Fire severity can result in top down effects in which differences in habitat conditions in burned environments can directly affect wildlife activity and browsing behavior. Alternatively, fire severity can influence browsing preferences and patterns indirectly through bottom up effects in which differences in soil hydrology, nutrient availability and light penetration based on burn severity can alter the growth patterns and defense strategies of regenerating aspen (Lindroth and St. Clair, this issue). Further research is needed to better understand how fire size and severity influence aspen susceptibility to browsing Trophic cascades involving ungulates in aspen communities Ungulate herbivory impacts on aspen communities can be altered by an apex predator. Trophic cascades are defined as an ecological relationship in which an apex predator directly affects the density and behavior of its primary prey (Paine, 1980). This relationship indirectly affects plants, via a release from herbivory (Paine, 1980). Trophic cascades research involving predator-ungulate-aspen interactions (Eisenberg et al., this issue) illustrates the complexity of the ecological impacts of herbivory on whole aspen communities. Most trophic cascade research involving aspen has been focused on wolf-elk-aspen interactions within national park systems (Hebblewhite et al., 2005; Ripple et al., 2001; White et al., 1998). This enables researchers to test for a clear herbivory signal without the influence of confounding variables such as hunting, land management, and domestic livestock. The YNP wolf reintroduction inspired dozens of trophic cascades studies, which have added significantly to our scientific understanding of aspen-ungulate interactions. Mixed-use landscapes (e.g., timber harvest, livestock grazing, hunting) add to the complexity of trophic cascades in these systems. Most aspen ecosystems are found on Bureau of Land management (BLM) and US Forest Service (USFS) land (Little, 1971), which contains livestock such as sheep and cattle, in addition to wild ungulates. Livestock can have significant negative impacts on aspen stands (Smith et al., 1972). Additionally, land management prescriptions and resource extraction can create complex trophic dynamics. Some researchers have capitalized on treatments such as timber harvest, ungulate grazing, and prescribed fire to design projects that explore a wide range of trophic interactions. For example, Bailey and Witham (2002) explored trophic cascades in aspen involving invertebrates in a mixed-use landscape. In highseverity fire sites, stands subjected to high levels of elk browsing had lower aspen regeneration and lower arthropod abundance. In intermediate-severity fire sites, intermediate levels of elk browsing demonstrated increased arthropod abundance. The leaf galler (Phylocopa bozemanii), was three times more abundant on unbrowsed ramets than browsed. Because leaf galling insects modify the environment and create shelters for other organisms, they have potential to be ecosystem engineers and keystone species. Thus it is important to understand the complex effects of variation on a particular system. Larsen and Ripple (2005) compared aspen demographics and the extent of aspen release on YNP s northern range on USFS land adjoining the park and evaluated the effects of elevation, late 19th century fires, and pre-fire forest composition on recruitment. They found recruitment of aspen into the canopy where browsing pressure has been reduced due to hunting by humans and an increase

6 6 S Trent Seager et al. / Forest Ecology and Management xxx (2013) xxx xxx of predation risk via the 1995/1996 wolf reintroduction. Kimble and others (2011), working in the same study area, conducted a 2006 resurvey of plots previously surveyed in 1991, prior to the wolf reintroduction. They found no significant change in the amount of elk browsing on aspen and continuing failure of aspen recruitment into the canopy, regardless of a high wolf population. In attempting to explain this lack of a trophic cascade (release in aspen indirectly mediated by wolves), Kimble and others (2011) speculated that the shift to a hotter, drier climate and fire suppression could be factors restricting aspen growth, making it more difficult for these stems to recruit above the browse height of elk. To better understand complex aspen-ungulate interactions, future trophic cascade research should include additional studies representing aspen ecosystems in mixed-use landscapes (Eisenberg, 2012) Human impacts Humans directly and indirectly modify ungulate herbivory on aspen. Such impacts include: land-use, such as extensive livestock grazing (Smith et al., 1972); fire suppression and alteration of fire regimes (White et al., 1998; Hessl, 2002); timber harvest (Binkley et al., 2006; Swanson et al., 2010); extirpation of large predators such as wolves (Leopold, 1943; Ripple et al., 2001); wild ungulate management for maximum sustained yield (Leopold et al., 1947; Vucetich et al., 2005; Wagner, 2006), and climate change (Rehfeldt et al., 2009; Worrall et al., 2010; Hanna and Kulakowski, 2012). Herbivory is more likely to be heterogeneous in areas that contain human hunters (White et al., 2003), wolves (Hebblewhite et al., 2005), coarse woody debris (Reynolds, 1969), and different aspen functional types (e.g., seral and stable) (Kurzel et al., 2007). Aldo Leopold suggested using hunting by humans to emulate hunting of ungulates by wolves (Flader, 1994). However, in practice, this generally has not occurred (Berger, 2005). Human firearms (e.g., use of scopes and high-powered rifles), strategies (taking prime animals), and season (limited and generally not occurring when game is the most concentrated) all differ from methods used by apex predators which keeps a more natural balance in ungulate population levels. The role of human hunting in ungulate management varies across western North America. Alaska Fish and Game are encouraged through political and societal processes to emphasize maximizing moose and other large ungulates for hunters (Boertje et al., 2010). Conversely, nearby British Columbia uses hunting as a tool for reducing moose populations for the recovery of caribou (Rangifer tarandus) and associated habitats (Serrouya et al., 2011). Western North America s mixed-use landscape contains an extensive road network, which alters elk herbivory via habitat fragmentation and elk displacement (Rowland et al., 2005). Wisdom and others (2004) found vehicle traffic and human presence could displace elk from habitats within their home range. Additionally, human recreational activities (all-terrain vehicle, biking and horseback riding) may negatively impact elk through decreased feeding time and increased travel time, (Rowland et al., 2005; Naylor et al., 2009), although no studies have been done specifically on how this may influence ungulate browsing impacts on aspen communities. 6. Management implications and strategies 6.1. Exclosures, refugia, and jackstraw Fig. 4. Aspen exclosure in Fishlake National Forest, Utah, showing prolific aspen sprout survival and density inside the exclosure but lacking where ungulates still have access. Photo: Bob Campbell, US Forest Service, Fish Lake National Forest. 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 Bartos, 1977; Loft et al., 1987; White et al., 1998; Zeigenfuss et al., 2008; Seager, 2010). In the Intermountain West, aspen sprouts and mature stems within ungulate exclosures were found to persist during drought and other climate-related events, while aspen not protected from chronic herbivory experienced stand decline (Baker et al., 1997; Kay and Bartos, 2000; Kay, 2001a). While it is not always economically feasible to use exclosures as a management tool at the landscape scale (Rolf, 2001), they play an important role in characterizing browse impacts in scientific studies (Martin and Maron, 2012). Refugia are areas on the landscape that naturally exclude ungulates across decades or centuries, and as such provide long-term data on tree recruitment and community structure in the absence of herbivory (Carson et al., 2005). Aspen refugia can function as baseline data for aspen recruitment (Ripple and Larsen, 2001; Shirley and Erickson, 2001; Larsen and Ripple, 2003). Jackstraw (e.g., heavy tree-fall) provides a management tool to deter ungulates and allow aspen recruitment. While exclosures and refugia are used to examine aspen regeneration and recruitment in the absence of ungulates, areas with jackstraw deter but do not entirely exclude ungulates. The complex piles of coarse woody debris characteristic of jackstraw can deter ungulate use of aspen stands, allowing a release of aspen sprouts and stem recruitment into the overstory (Reynolds, 1969; Halofsky and Ripple, 2008; Seager, 2010). However when post-fire herbivory is high, jackstraw alone does not deter elk from browsing aspen sprouts (Romme et al., 1995; Forester et al., 2007). Kota and Bartos (2010) found in cut aspen stands in South Dakota that slash-piles could deter livestock, but a more substantial barrier, such as aspen hinging, is needed to exclude elk and deer Seedling establishment and genetic diversity Establishment of new genotypes (seedlings) can be an important source of genetic variation that contributes to aspen resilience across its vast range (Leiffers et al., 2001; Frey et al., 2003; Mock et al., 2008; Worrall et al., 2008). Aspen seedlings have fewer resources than root-sprouts, and are less likely to survive ungulate browsing (Romme et al., 2005). In YNP, ungulate herbivory led to

7 S Trent Seager et al. / Forest Ecology and Management xxx (2013) xxx xxx 7 recruitment failure of new aspen seedlings in areas of high elk density (Forester et al., 2007; Romme et al., 2011). Swanson and others (2010) found newly established aspen seedlings inside dry forest exclosures 14 years after the fencing excluded ungulates. Land managers should recognize areas where disturbances, such as timber harvest and fire, remove surface organic layers and create potential aspen seed beds (Landhausser et al., 2010), and consider options for reducing high herbivory pressure in these areas to protect potential aspen seedlings and seed areas Fire and coppicing Overstory disturbances such as fire and clear-fell coppicing can induce root-sprouting of aspen (Shepperd, 2001). Disturbance and subsequent release of vegetation tends to attract elk and deer, resulting in severe impacts on aspen and suppression of growth of sprouts into the canopy (Baker et al., 1997). Thus, fire and coppicing alone will fail to create more resilient aspen communities without including some means to control ungulate herbivory. We recommend that prior to treating aspen stands with fire or clearfell coppicing, an evaluation of the ungulate population and its potential herbivory impacts be undertaken. An aspen restoration plan should include strategies to mitigate such impacts. These strategies might include exclosures, fencing, or leaving jackstraw in place (see Section 6.1). Additionally, in landscapes where apex predators exist, we suggest considering their role in managing aspen in fireprone systems (see Section 3). Measuring and managing ungulate populations is essential in order for fire, clear-fell coppicing, or other aspen treatments to succeed in meeting management objectives Restoring trophic cascades Forest management in a rapidly changing world must be informed by scientific understanding about conserving biologically and ecologically diverse ecosystems, while also meeting human needs. Such a vision would allow wolves and other apex carnivores to fulfill their ecological roles in helping restore and sustain resilient ecosystems, via trophic cascades. Current wolf pack presence substantially overlaps the distribution of aspen ecosystems in western North America (Little, 1971; USFWS et al., 2010). Given the body of science that suggests the potential role of the wolf in helping stimulate recruitment of aspen above browse height (Eisenberg et al., this issue), we recommend maintaining recovered wolf populations in aspen communities, wherever that is practical Big game management and hunting policy To be an ecological surrogate for hunting by apex predators (i.e., functional redundancy), hunting by humans must create a similar prey functional response, triggering a release of vegetation from herbivory. Whether contemporary hunting policies can be altered sufficiently to create such a response has been the subject of much discussion since Aldo Leopold s era (Debyle, 1979; Flader, 1994; Berger, 2005) and will undoubtedly continue to be so. Beyond the effect of natural processes, such as fire and predation, measuring elk densities with more uniform metrics on local, landscape, and regional scales represents another knowledge gap. Leopold (1943) attempted to do this in his work as a scientist and in his surveys as a manager. However, currently agencies do not employ standardized metrics within or among states, or a more holistic awareness of the effects of density, to maximize the usefulness of density measures. Understanding ungulate summer migration and winter range, along with population/density estimates, would allow scientists to place their aspen herbivory research into landscape and regional context. While the short-term, or decadal, impacts of ungulate herbivory on aspen are well known, the implications of longer-term, chronic browsing on aspen forest development and resilience are poorly understood. For example, we do not know what the long-term impacts will be (across multiple decades or longer) of an ungulate population maintained at historically unmatched density levels and being managed unsustainably (Rooney, 2001; Côté et al., 2004). Public support of high ungulate populations decreases when vegetation and habitat, such as aspen, are heavily impacted on the landscape (Fix et al., 2010). The US National Park Service (NPS) recently adopted a management strategy of restoring aspen and other vegetation communities by decreasing elk numbers inside RMNP via hunters and sharpshooters instead of apex predators (NPS, 2007). However, we know little about the sort of ungulate population reduction necessary to produce desired effects. For example, even a 30% reduction in elk numbers was insufficient to allow aspen recruitment on the Coccino National Forest in Arizona (Rolf, 2001; Zegler et al., 2012). Wildlife managers set ungulate population benchmarks for hunter satisfaction, using irruptive population numbers as a baseline. A new paradigm is needed, which would involve incorporating what we know today about the effect of keystone natural processes, such as predation and fire, to enable managers to maintain ungulates at appropriate levels. For example, an aspen system that has fire and predators in it may ultimately sustain a higher density of ungulates, because fire stimulates aspen regeneration and predators keep ungulates on the move (Eisenberg, 2012). We suggest that where possible managers allow apex predators to increase in number to the point that they are able to control wild ungulates via predation (density-mediated response) and via altered behavior (behavioral response) (Creel et al., 2005; Kauffman et al., 2007, 2010). 7. 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 manage aspen for greater resilience. To increase aspen resilience in the face of current and future environmental change, managers should focus on the survival and recruitment of aspen sprouts, young ramets, and seedlings by releasing them from chronic browsing. More research is needed to better determine sustainable herbivory levels from different ungulate suites on diverse landscapes. Herbivory is more heterogeneous in areas that contain human hunters, wolves, or fire on the landscape (White et al., 2003; Hebblewhite et al., 2005; Eisenberg, 2012). Thus a management approach that includes disturbance (e.g., fire), and predation on ungulates may increase aspen resilience. More research is needed outside of national parks on mixed-use landscapes to better understand how the presence of wolves and human hunters interact with herbivory impacts on aspen sprouts post-fire. The complexities of ungulate herbivory and fire on aspen ecosystems, especially in relation to scale, are not clearly understood. Wildlife agencies responsible for elk and deer populations should consider management strategies which use ungulate herbivory impacts on ecosystems such as aspen as indicators of sustainable herd densities. As outlined in this review, to increase aspen ecosystem resilience, we recommend a multi-faceted approach that involves enhancing bottom up forces while decreasing top down impacts from ungulates.

8 8 S Trent Seager et al. / Forest Ecology and Management xxx (2013) xxx xxx 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 their help and contribution of an aspen photo. Earlier drafts of this manuscript were reviewed by Dan Binkley and anonymous reviewers. Their insightful comments significantly helped improve this paper, and we thank them. References Aitken, K.E., Martin, K., Nest cavity availability and selection in aspen conifer groves in a grassland landscape. Can. J. 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