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13.1 13.1 Introduction

In recent years, conservation biologists broadened their efforts beyond genes, species, and ecosystems to include the conservation of species interactions such as mutualisms and predation (Kearns et al. 1998; Soulé et al. 2003, 2005). Ecologists generally agree that predators generate top-down effects in food webs, but the consensus ends there. Considerable disagreement remains over the strength of top-down effects, the relative importance of top-down versus bottom-up effects, and how the relative importance of these effects differs among systems, seasons and across scales (Polis 1999; Polis et al. 2000; Shurin et al. 2002; Schmitz et al. 2004). The question is further complicated because many top predators were significantly reduced in abundance or eliminated from temperate zone ecosystems decades or centuries before ecologists formally conceptualized trophic cascades (cf. Jackson 1997; Jackson et al. 2001). Still, many conservation biologists view the recovery of the gray wolf (Canis lupus) in the Great Lakes region as more than a conservation success story. This recovery carries with it the hope and expectation that the top-down effects generated by gray wolves will aid in the maintenance of regional biodiversity (McShea 2005; Ray 2005).

High densities of white-tailed deer (Odocoileus virginianus) throughout much of the upper Great Lakes region pose a challenge to conservation efforts. Densities are so great that deer harvests have set state records within the last 10 years (e.g., Michigan in 1998, Wisconsin in 2000, and Minnesota in 2003). High densities of deer come at an ecological cost: browsing contributed to the loss of plant diversity over the last few decades (Rooney et al. 2004), and, in turn, these losses might be generating additional indirect effects on insects, birds, and other species (Rooney and Waller 2003; McShea 2005). Several studies from western North America suggest that recovery of gray wolves generated strong top-down effects on vegetation and lateral effects on assemblages of scavengers (Ripple et al. 2001; Wilmers et al. 2003; Hebblewhite et al. 2005).

Are wolves having a similar effect in the Great Lakes states? While it might be tempting to simply extrapolate findings from western North America and apply them to this region, doing so would gloss over several important differences. Elk (Cervus elaphus) serves as the primary prey species in western North America, whereas white-tailed deer (and on Isle Royale, moose, Alces alces) is the primary prey of wolves in the Great Lakes states. White-tailed deer and moose are browsers, feeding primarily on forbs and woody plants. Elk rely on a mixed foraging strategy that includes both browsing and grazing, relying more heavily on grasses and other graminoid plants (Gordon 2003). Because their food resources are distributed differently in both space and time, the spatial distribution and behavior of these ungulates differs as well. Elk tends to be more social than white-tailed deer or moose (Kurta 1995). In western North America, high-quality browse is concentrated in riparian areas, but in the Great Lakes states, it is more evenly distributed throughout the landscape. Elk and white-tailed deer also differ in their seasonal movements. Elk migrate to their winter range each year, whereas migration of deer to winter yards varies annually in response to winter severity, and geographically, as the severity of winters is more pronounced toward the northern limits of the geographic range of deer.

The Great Lakes states lack the topographic relief and the extensive open grasslands of the Rocky Mountain region, and both could influence predator–prey dynamics. The more open, rugged landscapes of the west make it easier for wolves to locate prey. The food web structures also are very different between the regions. Western North American food webs contain more ungulates and predators than those in the Great Lakes states. Smith et al. (2003) showed greater complexity of food webs in Yellowstone National Park than on the smaller and more depauperate Isle Royale. While food web structure on the mainland in the Great Lakes states is more complex than on Isle Royale, it still lacks the complexity of Yellowstone (compare Smith et al. 2003 with Kurta 1995). The Great Lakes region also contains higher densities of people and roads. For these reasons, findings from the west might not be directly applicable to the Great Lakes states. However, insights from western North America do provide a starting point for trying to understand what, if any, trophic effects wolves may have in the Great Lakes region.

In this chapter, we explore the trophic effects that wolves have in Yellowstone National Park and the northern Rocky Mountains. We combine this body of research with studies conducted in the Great Lakes region, identifying trophic interactions that are common to both regions. We highlight some of the important factors that can modulate trophic effects in the Great Lakes region, and conclude with predictions how these trophic relationships will play out over time, and the research needed to test these predictions.

13.2 13.2 Trophic Interactions and Subsidies of Scavenger Food Webs

Soulé et al. (2003) consider the wolf to be a “strongly interactive” species, meaning that its removal or substantial reduction leads to significant changes in the ecosystems it inhabited. Their terminology is similar to Paine's (1966) keystone species concept, but it relaxes the requirement that the species has effects disproportionate to its population density. Evidence from western North America and the Great Lakes region support the idea that the wolf is strongly interactive and influencing biodiversity at some scales.

13.2.1 13.2.1 The Wolves of Yellowstone National Park and the Northern Rocky Mountains

Absent since 1926, wolves were reintroduced to Yellowstone National Park in 1995. Elk served as their primary prey, and White and Garrott (1995) reported that in their first decade of recovery, wolves had no appreciable effect on densities of mule deer (Odocoileus hemionus), bison (Bison bison), moose, bighorn sheep (Ovis canadensis), or pronghorn antelope (Antilocapra americana). They further noted a 50% decline in population density of elk between 1995 and 2004, suggesting a pronounced effect of wolves on elk. This precipitous decline, however, also may have been influenced by coincident extreme weather events and increased harvest rates by humans (Vucetich et al. 2005).

Studies of the age structure of trembling aspen (Populus tremuloides) and cottonwood (Populus) trees revealed a more-or-less regular pattern of establishment, until wolves were extirpated. A significant gap in establishment stretches from the 1920s through the 1990s, a period marked by intense herbivory by elk (Beschta 2003, 2005; Larsen and Ripple 2003). Released from herbivory, heights, and densities of riparian aspen, cottonwood, and willow (Salix) seedlings increased (Ripple et al. 2001; Ripple and Beschta 2003, 2006, 2007; Beyer et al. 2007). Declines in elk density probably contributed to this recovery, but only in part. Foraging elk exhibited increased vigilance (Fortin et al. 2004) and selected summer habitats in areas that offered increased protection from wolves (Mao et al. 2005). Recovery of vegetation was most pronounced on sites where predation risk was highest (Ripple and Beschta 2003), suggesting that trophic cascades were mediated through prey behavior (Ripple and Beschta 2004; Fortin et al. 2005). When elk detect wolf activity, they become more wary and tend to avoid high-risk sites. The combination of increased vigilance, forgoing feeding opportunities where they would be vulnerable to predation, and frequent movement through the landscape dilutes browsing pressure on the landscape, enabling woody plants that were suppressed by browsing to begin recovery (Gude et al. 2006).

Recovering vegetation can lead to additional indirect effects on other species (Berger and Smith 2005). Berger et al. (2001) compared the consequences of the loss of predators in Grand Teton National Park, where hunting was not permitted, to those in control sites with human hunting pressure. In addition to noting greater densities of moose and lower heights and densities of willows, densities of birds were lower in riparian areas without human hunting pressure. Hebblewhite et al. (2005) found similar patterns in Banff National Park: in areas where densities of wolves were low, they observed higher densities of elk, lower net twig production by willows, and lower density and diversity of songbirds. They further noted a decrease in abundance of beaver (Castor canadensis) lodges in areas with high densities of elk, providing evidence of a positive, indirect effect of wolves on beavers.

Top-down effects of wolves have not been uniform throughout the region. Garrott et al. (2005) noted that densities of elk varied substantially between two areas 30 km apart in the Madison watershed, despite both having resident wolf packs. Ripple and Beschta (2007) found significant recovery of aspen in riparian areas and wet meadows, but not in upland steppe habitats. In another study, they reported recovering willows were evident in valley bottoms, but not in upland riparian areas (Ripple and Beschta 2006). With respect to both prey and trophic cascades, the effect of wolves has been strongly context dependent.

In addition to generating top-down effects, wolves can generate lateral effects by influencing scavenger food webs. Prior to reintroduction of wolves, availability of carrion was a function of winter severity and consequently was concentrated in late winter (Wilmers et al. 2003). Following the recovery of wolves, carrion became more abundant throughout most of the winter, potentially benefiting populations of other scavengers, including ravens (Corvus corax), golden eagles (Aquila chrysaetos), bald eagles (Haliaeetus leucocephalus), red foxes (Vulpes vulpes), black-billed magpies (Pica hudsonia), and numerous species of carrion-feeding insects. By decreasing inter-annual variation in the availability of carcasses, wolves could contribute to larger population sizes of scavengers. Wilmers et al. (2003) proposed that the growth in other scavenger populations could decrease the amount of food wolves derive from each kill, forcing them to kill more frequently and therefore strengthening top-down effects.

13.2.2 13.2.2 Wolves of the Great Lakes States

Wolf populations showed significant increases in Minnesota in the 1960s, Wisconsin and northern Michigan in the 1990s and early 2000s (Mladenoff et al. 1997; Erb, this volume; Wydeven et al., this volume; Beyer et al., this volume). There are few examples of systems where wolves limit prey densities in the region, but one such situation occurs at the northern limit of the geographic range of white-tailed deer in Minnesota (Nelson and Mech 2006). Eberhardt (1997) noted that it was difficult to assess the effects of wolves on moose on Isle Royale, but concluded that it was possible for wolves to limit prey populations (see also Mech and Peterson 2003; Vucetich and Peterson, this volume).

Trophic cascades attributed to large carnivores have been detected in the Great Lakes region, although the amount of research has been limited (Ray et al. 2005). One of the first studies to convincingly demonstrate a trophic cascade in terrestrial ecosystems came from the wolf–moose–balsam fir (Abies balsamea) system on Isle Royale (McLaren and Peterson 1994). Here, greater annual-increment growth rings of balsam fir corresponded with periods of high density of wolves and low density of moose, indicating a release from browsing pressure. Qualitative observations from northeastern Minnesota revealed greater recruitment of saplings in the swath of a tornado in areas with few deer and large wolf populations, compared to adjacent areas with more deer (Nelson and Mech 2006). D. P. Anderson et al. (unpublished data) found that forbs, shrubs, and saplings had higher biomass in cedar swamps located within territories of wolf packs, but this effect was not detected in three other forest types. Their study was conducted in Wisconsin and parts of western Michigan, where white-tailed deer depress forage productivity and biomass in cedar swamps (Rooney et al. 2002). Evidence for trophic cascades following wolf recovery in the Great Lakes region has not been as strong as the evidence uncovered in the Rocky Mountains region, but this seems more to do with absence of evidence rather than evidence of absence. We are not aware of any studies in the Great Lakes region that examine trophic cascades beyond responses of vegetation.

There is compelling evidence that wolves generate behavioral shifts in their prey in the Great Lakes region, as reported for western North America. In his study of a rapid decline in prey density, Mech (1977) observed that the majority of surviving white-tailed deer were found at the edges of wolf-pack territories. Mech hypothesized that where wolf-pack territories abut, conflicts between packs create a buffer zone that can serve as a refuge for prey. Later research confirmed that these buffer zones do support higher densities of deer (Rogers et al. 1980) because wolves experience higher mortality rates near the edge of their territory as a result of conflicts with neighboring packs (Mech 1994). In their study of a small, reintroduced herd of elks, Anderson et al. (2005) reported that the location of wolf packs influenced habitat selection of individual elk at broad spatial scales; elk established home ranges in areas away from wolves.

There has been no research specific to the Great Lakes region on how wolves might generate lateral effects to influence scavenger food webs, but it is likely to differ substantially from what other researchers observed in western North America. Collisions with vehicles are an important source of mortality for deer in Wisconsin and Michigan, and probably play a more important role in subsidizing scavenger food webs than wolves. Species tolerant of edges and traffic like ravens and crows (Corvus brachyrhynchos) are more likely to benefit than less-tolerant species. Populations of wolves in the Great Lakes region still subsidize scavengers, but their importance to this food web is probably less than in the west.

13.3 13.3 Factors Modulating Tropic Interactions

Over the last decade, researchers have shifted from asking whether trophic cascades operate in terrestrial systems to understanding the strength and importance of trophic cascades in different contexts and under different conditions (Pace et al. 1999; Polis et al. 2000). Spatial variation in top-down effects appears both in western North American and in the Great Lakes ecosystems. In Yellowstone National Park, for example, some of this variation is due to perceived predation risk (Ripple and Beschta 2003). In fact, several factors can act to modulate the strength of trophic interactions.

Variation in climate appears to be one such factor in the Great Lakes region. Wolf–moose dynamics on Isle Royale in winter are mediated by snowfall. In years with high snowfall, wolves hunt in larger packs and per capita kill rates rise. Moose density shows a negative correlation with the average size of wolf packs in the previous winter, and annual growth of balsam fir increases with decreasing moose density (Post et al. 1999). The coupling between climate and strength of trophic interactions has important consequences with respect to climate change. If climate change leads to milder winters with less snowfall, the magnitude of this trophic cascade will probably weaken, all else being equal.

Climate also affects scavenger food webs in Yellowstone National Park. Wilmers and Getz's (2005) model predicts that a reduction in snow depth as a result of climate change will enhance survival of elk in winter. As a consequence, availability of carrion in late winter may decline in the future relative to today. The model predicts more carrion with wolves than without, but climate could become an overriding factor.

Parasites also can play an important role in community dynamics of predators (Hatcher et al. 2006), potentially modulating the strength and importance of trophic cascades. For example, Wilmers et al. (2006) examined an outbreak of canine parvovirus (CPV) on Isle Royale and its effects on wolves, moose, and balsam fir. Following the introduction of CPV, the wolf population declined numerically. This decline in the abundance of wolves diminished the importance of predation in moose population dynamics, resulting in an increase in the relative importance of bottom-up population regulation. CPV has probably also contributed to reduced growth rates of balsam fir through its direct effects on wolves and indirect effects on moose (McLaren and Peterson 1994). Perhaps most interesting, Wilmers et al. (2006) found that the relative importance of climatic variation as a determinant of moose population growth rates doubled after the introduction of CPV, reflecting complex interactions involving climate, parasites, and trophic cascades.

Habitat productivity also can modulate the strength of trophic interactions and indirect effects in ecosystems. In their study of herbivore-generated indirect effects in a tropical savanna, Pringle et al. (2007) found strong direct effects of ungulates on productivity of vegetation and significant indirect effects on lizards and arthropods. The strength of these indirect effects increased with decreasing productivity. How wolf-generated trophic cascades might vary across productivity gradients has not been explored in detail.

Recent work by Schmitz et al. (2004) on arthropod assemblages highlights the importance of food web topology as a mediator of trophic cascades. Depending on the particular configuration of the food web, predators can have both positive and negative effects on plants in systems where predators influence prey behavior.

Finally, human activities can modulate the strength of trophic interactions through a variety of mechanisms, only a few of which we will highlight. In the Great Lakes region, white-tailed deer serve as the primary prey for wolves. Human hunters and vehicular collisions are major sources of deer mortality, but are unlikely to reduce the wolf's prey base substantially. It is not clear if the human toll causes additive or compensatory mortality, although research from Yellowstone National Park found compensatory mortality in the elk population subjected to depredation by both humans and wolves (Vucetich et al. 2005). Other activities, though, can enhance this prey base. The fragmentation of land ownership creates a mosaic in which some land is accessible to deer hunters, while other land is not. Furthermore, firearms ordinances create safe havens for deer in municipal areas. Humans can increase availability of forage for deer at multiple scales: recreational feeding increases concentrations of deer locally, intensive forestry and crop production can boost carrying capacity regionally. Finally, human activities influence many other modulators already mentioned, including climate, introductions of disease, and habitat productivity.

13.4 13.4 Trophic Interactions of the Recovered Great Lakes Wolf Population: Predictions and Research Needs

Ray (2005) questioned whether wolf recovery in eastern North America would influence deer populations and generate the trophic cascades now demonstrated in Yellowstone National Park. We believe that they will under some but not all conditions. Where trophic cascades do occur, we expect them to be almost exclusively through the behavioral effects on prey, rather than through a numerical effect. By increasing vigilance and movement of prey (Switalski 2003; Fortin et al. 2004; Gude et al. 2006), wolves may generate increases in biomass and productivity of some plant species in some places. However, the strength and importance of this effect will be modulated by climate, human activity, habitat productivity, and several other factors. The challenge will be predicting where and when trophic cascades will be important.

Where should we look for trophic cascades? The recolonization of the Great Lakes region by wolves has superimposed a type of chronosequence on the land. Packs became established in some areas 15 years ago, other areas 10 years ago, and still others only 5 years ago. Some areas remain uncolonized and will likely remain so. By conducting studies close to the core of wolf-pack territories in each of these areas and holding habitat constant, we can begin to look at differences in sapling, shrub, and herbaceous vegetation as a function of time since colonization by wolves. Alternatively, we can study vegetation in the buffer zones between packs and compare it to vegetation within an identical habitat type within territories. Both approaches might be combined with deer exclosure experiments to examine differences in plant performance in areas with and without wolves. These approaches provide a natural experimental framework to identify what, if any, effects wolves are having on vegetation.

The snow depth gradient that decreases from Lake Superior south to Wisconsin and Michigan's Upper Peninsula provides another research opportunity. Since per capita kill rates increase with snow depth, wolves might generate trophic cascades by reducing winter deer densities close to Lake Superior where snows are deepest.

What should we look for? The wolf-generated trophic cascades described thus far have been what Polis (1999) terms species cascades, that is, affecting one or a few specific species of plants. In some contexts, wolves have facilitated increased growth rates of aspen, willow, cottonwood (Ripple and Beschta 2003, 2006; Hebblewhite et al. 2005; Beyer et al. 2007), and balsam fir (McLaren and Peterson 1994). Researchers should initially identify trophic effects on the size or reproductive status of individual plant species impacted by deer overbrowsing. Ideally, these species should be fairly widespread. Candidate species include northern white cedar (Thuja occidentalis), bluebead lily (Clintonia borealis), hairy Solomon's seal (Polygonatum pubescens), and sessile bellwort (Uvularia sessilifolia). Alternatively, researchers might look to a guild of plants likely to generate indirect effects. Rooney et al. (2004) observed declines in the relative frequency of plant species with animal-pollinated flowers where impacts of deer browsing were most pronounced. This could have indirect consequences for insect pollinators. It seems unlikely that wolves will generate trophic cascades strong enough to affect overall primary productivity, as there are some groups of plants such as graminoids that benefit under intense browsing pressure (Boucher et al. 2004).

Should we look for trophic interactions that are mediated via a numerical or behavioral response to wolves? Evidence from Yellowstone National Park suggests both numerical and behavioral trophic effects. Prior to reintroduction of wolves into Yellowstone in 1995, the northern range of the park harbored a very large elk population (19,000 elk; White and Garrott 1995). This population was unhindered in its movement and foraging, which took its toll on sensitive vegetation communities (Ripple et al. 2001; Ripple and Beschta 2003). Concurrent with the precipitous decrease in numbers of elk following the reintroduction of wolves (8,335 elk in 2004; White and Garrott 1995) were changes in the movement and foraging behavior of elk (Fortin et al. 2005; Mao et al. 2005). Consequently, it remains unclear in Yellowstone if the strong trophic effects are mediated primarily via numerical or behavioral responses. In contrast, the population size of white-tailed deer in the forests of northern Wisconsin at the onset of recolonization by wolves was approximately 250,000 deer (WiDNR 1999). The population of deer has increased concurrently with the increasing wolf population to an estimated 365,120 deer in 2005 (Rolley 2005). The deer population is primarily controlled by winter severity and human harvest (Creed et al. 1984; WiDNR 1999), and with the possible exception of deer residing in the Lake Superior snow belt, the numerical effect of wolves on deer is clearly minimal. Trophic effects of wolves extending to plant communities in Wisconsin are, therefore, likely mediated via a behavioral response.

Despite decades of research, scientists are only beginning to understand the complex role wolves play in ecosystems. Even after 40 years, ongoing studies of the wolves and moose on Isle Royale yield surprising insights (cf. Post et al. 1999; Wilmers et al. 2006). The recent recovery of wolves in the Great Lakes region presents us with a unique opportunity, a chance to understand how a top predator influences biodiversity on a regional scale. We have not yet even scratched the surface, and the most exciting discoveries still lie ahead.