Wolves and the Ecology of Fear: Can Predation Risk Structure Ecosystems?: William J. Ripple & Robert L. Beschta (2004)

Abstract:

"We investigated how large carnivores, herbivores, and plants may be linked to the maintenance of native species biodiversity through trophic cascades. The extirpation of wolves (Canis lupus) from Yellowstone National Park in the mid-1920s and their reintroduction in 1995 provided the opportunity to examine the cascading effects of carnivore–herbivore interactions on woody browse species, as well as ecological responses involving riparian functions, beaver (Castor canadensis) populations, and general food webs. Our results indicate that predation risk may have profound effects on the structure of ecosystems and is an important constituent of native biodiversity. Our conclusions are based on theory involving trophic cascades, predation risk, and optimal foraging; on the research literature; and on our own recent studies in Yellowstone National Park. Additional research is needed to understand how the lethal effects of predation interact with its nonlethal effects to structure ecosystems."

Introduction
"The role of predation is of major importance to conservationists as the ranges of large carnivores continue to collapse around the world. In North America, for example, the gray wolf (Canis lupus) and the grizzly bear (Ursus arctos) have respectively lost 53% and 42% of their historic range,with nearly complete extirpation in the contiguous 48 United States (Laliberte and Ripple 2004). Reintroduction of these and other large carnivores is the subject of intense scientific and political debate, as growing evidence points to the importance of conserving these animals because they have cascading effects on lower trophic levels. Recent research has shown how reintroduced predators such as wolves can influence herbivore prey communities (ungulates) through direct predation, provide a year-round source of food for scavengers, and reduce populations of mesocarnivores such as coyotes (Canis latrans) (Smith et al. 2003). In addition, vegetation communities can be profoundly altered by herbivores when top predators are removed from ecosystems, as a result of effects that cascade through successively lower trophic levels (Estes et al. 2001). The absence of highly interactive carnivore species such as wolves can thus lead to simplified or degraded ecosystems (Soulé et al. 2003). [...]"

Figure 2. Elk browsing among cottonwood trees in the wintertime along the

Lamar River in the northern range of Yellowstone National Park during the

period when wolves had been extirpated. Note the lack of recruitment of

small and intermediate-sized cottonwood trees that has occurred over many

decades and the general lack of vigilance indicated by the elk.

Photograph: Yellowstone National Park.

Trophic cascades

"[...] A trophic cascade is the “progression of indirect effects by predators across successively lower trophic levels” (Estes et al. 2001). [...]

[...] Predators obviously can influence the size of prey species populations through direct mortality, which, in turn, can influence total foraging pressure on specific plant species or entire plant communities. [...]

[...] Changes in prey behavior due to the presence of predators are referred to as nonlethal effects or predation risk effects (Lima 1998). These behavioral changes reflect the need for herbivores to balance demands for food and safety, as described by optimal foraging theory (MacArthur and Pianka 1966). They include changes in herbivores’ use of space (habitat preferences, foraging patterns within a given habitat, or both) caused by fear of predation (Lima and Dill 1990). [...]

[...] Predation risk can also have population consequences for prey by increasing mortality, according to the “predationsensitive food” hypothesis (Sinclair and Arcese 1995). This hypothesis states that predation risk and forage availability jointly limit prey population size, because as food becomes more limiting, prey take greater risks to forage and are more likely to be killed by predators as they occupy riskier sites. Wolves have been largely absent from most of the United States for many decades; hence, little information exists on how adaptive shifts in ungulate behavior caused by the absence or presence of wolves might be reflected in the composition and structure of plant communities."

Figure 4. Flow diagram of predator–prey encounters for wolves and elk inYellowstone National Park (YNP) since 1926.Modified from Lima and Dill (1990).

Prey and plant refugia. "Prey refugia are areas occupied by prey that potentially minimize their rate of encounter with predators (Taylor 1984). For example, in a wolf–ungulate system, ungulates may seek refuge by migrating to areas outside the core territories of wolves (migration) or survive longer outside the wolves’ core use areas (mortality) (Mech 1977). [...]

[...] In national parks where both recreational hunting and large carnivores have been removed, dramatic changes in mammal and plant populations have been described (White et al. 1998, Soulé et al. 2003). [...]

Terrain fear factor. "The “terrain fear factor” (Ripple and Beschta 2003) represents a conceptual model for assessing the relative predation risk effects associated with encounter situations. This concept indicates that prey species will alter their use of space and their foraging patterns according to the features of the terrain and the extent to which these features affect risk of predation (e.g., avoid sites with high predation risk; forage or browse less intensively at high-risk sites). [...]

Predation risk in a dynamic environment. Environmental variables that may influence the degree of predation risk include winter weather, wildfire, and the depth and spatial distribution of snowpacks. Snowpack conditions can greatly influence ungulates’ access to vegetation (both herbaceous and woody species) and thus their starvation rates.Variations in snow depth can also affect the ability of ungulates to escape predators (Crête and Manseau 1996). For example, wolves have been found to have higher ungulate kill rates when snow is deep compared with times when snow is shallow (Huggard 1993, Smith et al. 2003). [...]

Ecosystem responses. Ecosystem responses to trophic cascades can be many and complex (Estes 1996, Pace et al. 1999), but for simplicity we focus on riparian functions and on beaver (Castor canadensis) and bird populations. We acknowledge that trophic cascades can affect many other aspects of ecosystem structure and function, both abiotic and biotic, including habitat for numerous species of vertebrates and invertebrates, food web interactions, and nutrient cycling (Rooney and Waller 2003). [...] Researchers have recently made connections between the loss of large carnivores and decreases in avian populations. The local extinction of grizzly bears and wolves in Grand Teton National Park caused an increase in herbivory on willow by moose and ultimately decreased the diversity of Neotropical migrant birds (Berger et al. 2001)."

Figure 5. Trophic interactions due to predation risk and selected ecosystem responses to (a) wolf extirpation (1926–1995) and (b) wolf recovery (post-1995) for northern ecosystems of Yellowstone National Park. Solid arrows indicate documented responses; dashed arrows indicate predicted or inferred responses.

The Yellowstone experiment

"In the discussion below of recent research results from YNP, we describe the northern winter range ecosystem, historical predator–prey–vegetation dynamics, and changes in the northern range environment since wolf reintroduction in 1995. Not only is the northern range a sufficiently large ecosystem for assessing trophic cascade effects, the role of elk relative to woody browse species has been a topic of concern over many decades. [...]

Northern winter range. The northern winter range comprises more than 1500 km2 of mountainous terrain, of which approximately two-thirds occurs within the northeastern portion of YNP in Wyoming (NRC 2002a). [...]

Yellowstone from the 1800s to 1995. Relatively little is known about the occurrence of carnivores and ungulates in northwestern Wyoming in the early 1800s or the effects of hunting and fire use by Native Americans. Even with the advent of Euro-American beaver trappers in the mid-1800s, little information about the biota of the northern range was systematically recorded. Although YNP was established in 1872, uncontrolled market hunting inside and adjacent to the park had significant effects on both carnivore and ungulate populations in the early years of park administration. To help curtail impacts on wildlife and other resources, in 1886 the US Army assumed responsibility for protecting resources within the park.Ungulates, bears, and beaver were generally protected during the period of army administration, which ended in 1918; however, predators other than bears were typically killed. [...]

[...] Viewed from a perspective of trophic cascades and predation risk, the plant community responses experienced in northeastern YNP over the 20th century are consistent with the expected consequences of extirpating gray wolves. The resultant lack of predation and predation risk allowed elk to forage unimpeded on woody browse species, causing much-simplified plant communities of low stature (figure 4). Without the presence of this keystone predator, the only major limitation to accessing woody browse species each winter was snow depth. [...] The loss of beaver populations appears to represent an ecological chain reaction to behaviorally mediated trophic cascades involving elk, following the extirpation of wolves. According to the NPS (1961), the decrease in beaver in the northern range, which began in the late 1920s, resulted from interspecific competition with elk: Beaver would fell the larger stems of aspen, willow, or cottonwood for food and dam material, while elk would consume all new shoots. Thus, unimpeded browsing by elk may have effectively destroyed any food supplies for beaver. [...]

Figure 6.Willow along Blacktail Creek in spring 1996 (left) and summer 2002 (right). Following a 70-year period of wolf extirpation, heavy browsing of willows and conifers is evident in the 1996 photograph. In 2002, after 7 years of wolf recovery, willows show evidence of release from browsing pressure (increases in density and height). Photographs: left, Yellowstone National Park; right,William J. Ripple.

Yellowstone after wolf reintroductions (1995–present). Under the protection of the 1973 federal Endangered Species Act, an experimental population of wolves was reintroduced into YNP during the winter of 1995/1996, following a 70-year period without their presence (figure 1a). Since the reintroduction of 31 wolves into YNP in the mid-1990s, their numbers have steadily increased. By the end of 2001, the population of wolves in Yellowstone’s northern range had grown to 77 animals (Smith et al. 2003). Even with the reintroduction of wolves and their subsequent increase in recent years, we are still in the early stages of understanding how their restoration is influencing ungulates, vegetation, riparian functions, or other ecological components in northern Yellowstone (figure 5b).

Following the reintroduction of wolves, Ripple and Beschta (2003) found that predation risk associated with various terrain conditions (and their related fear factors) played a role in the selective release of willow and cottonwood from the browsing pressure caused by elk in the Lamar Valley of northern YNP. In 2001 and 2002, they found willow and young cottonwood plants 2 to 4 m in height, which is in stark contrast with the long-term observations of plants less than 1 m in height during the decades before wolf reintroduction. Willow and cottonwood were found to be subject to less browsing pressure (figure 6) at potentially high-risk sites with limited visibility (i.e., limited opportunities for prey to see approaching wolves) or with terrain features that could impede the escape of prey, such as sites below high terraces or steep cutbanks and near gullies. [...]"

Conclusions
"Can predation risk structure ecosystems? Our answer—based on theory involving trophic cascades, predation risk, and optimal foraging, in addition to a developing body of empirical research—is yes. Although some may find the support for this answer equivocal, we find it compelling when all the evidence is combined. Predation risk probably affects ecosystems in both subtle and dramatic ways through various interactions, many of which are unknown. [...] In Yellowstone, the role of lethal effects may become increasingly important in the future, as the combined effects of predation by wolves, bears, and hunters, along with periodic severe winter weather events, may ultimately cause lower elk populations. [...]  the extirpation of the gray wolf—a keystone predator in this ecosystem—is most likely the overriding cause of the precipitous decline and cessation in the recruitment of aspen, cottonwood, and willow across the northern range. [...] 

[...] In terms of future management of the northern range ungulate herds, our assessment suggests that restoration goals should focus on the recovery of natural processes. In the case of Yellowstone, the return of wolves represents an example of active management to recover a lost keystone species. [...]

[...] Since much of our discussion has focused specifically on the northern range of YNP, we are not sure of the extent to which our conclusions on behaviorally mediated trophic cascades match what has occurred to ungulates, plants, and associated ecosystem responses in other portions of North America where wolves have been extirpated and, in some cases, reintroduced. In the last decade, wolf recovery efforts have been initiated in portions of Montana, Idaho, Arizona, New Mexico, and the upper Midwest. If ecosystem responses similar to those that have occurred historically or that are under way on the northern range are documented in other locations, we may finally understand more fully the observations and concerns of Aldo Leopold from over half a century ago."
  

Wolves and the Ecology of Fear: Can Predation Risk Structure Ecosystems?: William J. Ripple & Robert L. Beschta (2004) http://bit.ly/OOu9w1 BioScience, 54(8):755-766. 2004. Published By: American Institute of Biological Sciences: http://www.bioone.org/