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Identifying and understanding the trophic links between carnivore and herbivore guilds is critical to understanding predator–prey relations and community diversity. To this end, ecologists have traditionally focused on the effects of predator foraging behaviour as they cascade down the food chain. As a major predator of large ungulates, grey wolves may suppress prey levels or alter prey behaviour to the extent that they affect vegetation patterns and productivity. On Isle Royale in Lake Superior, wolf predation on moose Alces alces (L.) has been shown to increase balsam fir Abies balsamea (L.) productivity (McLaren & Peterson 1994). In the long absence of wolves from the Greater Yellowstone ecosystem, moose populations flourished, reducing willow structure and density and subsequently decreasing the number of avian neotropical migrants which nest and feed in riparian areas (Berger et al. 2001). Since wolf reintroduction to Yellowstone National Park (YNP), changes in elk foraging have resulted in the release of aspen Populus tremuloides (Michaux) populations in some areas (Ripple et al. 2001). While trophic cascades are a well-documented mechanism by which top predators affect community process and pattern (Power 1992), less is known about the influence of top predators on fellow guild members. Here we show that grey wolves affect other meat eating species by subsidizing them with scavenge from their kills.
Recent work on resource subsidies has revealed that allochthonous input from more productive habitats may subsidize consumers in adjacent less productive habitats (Polis & Hurd 1995). Riparian lizards Sceloporus occidentalis (Baird) in California, for instance, have been shown to exhibit higher growth rates in near river habitats where aquatic insect densities are high (Sabo & Power 2002). While such resource flows from high productivity to low productivity habitats have been well documented (Fagan, Cantrell & Cosner 1999), little is understood about the possible mechanisms and effects of resource exchange from highly productive time periods to a less productive ones. Such temporal subsidies are common in agricultural settings where crop watering occurs during dry periods or livestock is fed during the winter, but its occurrence in nature is not well documented.
Prior to wolf reintroduction in YNP, carrion availability was primarily a function of winter severity (Gese, Ruff & Crabtree 1996). Specifically, high snow levels and cold temperatures caused elk to weaken and die, usually at the end of winter (Gese et al. 1996). Since wolves were reintroduced to Yellowstone in 1995, however, scavenging occurs at wolf kill-sites on a year-round basis (C. C. Wilmers et al. personal observation). By changing the distribution and abundance of carrion availability, wolves may serve to facilitate the acquisition of food by scavengers.
Carrion is crucial to the growth and fitness of many species in the Northern Rocky Mountains. Coyotes Canis latrans (Say) are highly dependent on winter scavenge (Crabtree & Sheldon 1999a) and have been shown to track wolves to their kill-sites and feed despite a high risk of predation (Paquet 1992). In addition, Crabtree & Sheldon (1999b) have shown that additional elk carrion increases coyote litter size and pup survival. Raven Corvus corax (L.) reproduction is tied to the availability of winter carrion (Newton, Davis & Davis 1982) and they adopt a foraging strategy of following wolves to locate their kills (Stahler, Heinrich & Smith 2002). Grizzly bears Ursus arctos (L.) are similarly dependent on spring carrion and are even known to forego hibernation altogether in Glacier National Park, Montana in favour of scavenging wolf kills (D. Boyd personal communication).
A group of grey wolves does not always fully consume their prey in one feeding (Mech 1970). Once satiated, they may stay to guard the carcass (Peterson 1977) and incur energetic costs associated with defence against scavengers or risk being killed by other predators such as grizzly bears and humans (Mech 1970). Alternatively, wolves may abandon the carcass and risk losing potential calories to scavengers. These costs must be balanced against the corresponding energetic output and risk of injury in acquiring their next prey item. If the cost of attaining a future prey item is less than the cost of remaining at the current carcass, wolves should abandon their kill. Partial consumption of prey by wolves has previously been linked to wolf-pack size, prey size (Paquet 1992) and winter severity (Mech et al. 2001) but little is known about the relative importance of these variables, the amount of carrion that wolves provide to other species, and how it is distributed throughout the year.
By directly observing wolves killing and consuming elk, we investigated the factors that determine partial consumption by wolves and the amount of carrion biomass they leave behind to the scavenger guild. We then use these factors to estimate the quantity and timing of this wolf-provisioned carrion subsidy to examine whether wolves have altered the temporal distribution of carrion availability to scavengers. We hypothesize that wolves (1) increase the abundance, (2) alter the timing, (3) decrease year-to-year variation and (4) change the source of the variance of carrion resource to scavengers. With its wide, open valleys, Yellowstone provides an excellent opportunity to observe wolves preying and feeding on ungulates, which has not existed in other studies where inaccessibility or forest cover severely limited viewing possibilities (e.g. in Minnesota, Denali, Isle Royale, Elsmere Island, Algonquin).
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We observed 240 wolf-killed elk carcasses during the study period for a total of 104 640 min. Fifty-seven of these carcasses were observed from beginning or near beginning (during stage 1 and only wolves had fed) to end of consumption during the winter period of 1 November to 1 April: 8 of these were bulls, 24 were cows, 24 were calves and 1 was unknown. Estimated carcass masses varied from 101 to 269 kg and were located between 30 and 3250 m from the road. Wolf-group size at carcasses ranged from 1 to 27 animals. Other major consumers of these carcasses included coyotes, grizzly bears, ravens, magpies, bald eagles and golden eagles.
Measurements of bird ACR on muscle were significantly different from ACR on bone for ravens (P = 0·03, Table 2) and for magpies (P = 0·04, Table 2). Elk dissection revealed that approximately 68% of an elk's whole mass is edible. Approximately 14% of the elk's whole mass is in stage 1, 31% in stage 2, 15% in stage 3 and 6% in stage 4 (Table 1). The remaining 32% comprises rumen and inedible bone.
The percentage of the carcass consumed by wolves was significantly predicted by six variables on their own: WPKP, PACKS, PREYM, SWE, TMIN and ROAD (Table 3). As pack size increases, the percentage consumed by a wolf pack also increases (Table 3). As prey mass increases, percentage consumption decreases (Table 3) because the wolves become satiated before fully consuming the carcass. WPKP explained more of the variation in percentage consumption than any other variable alone (r2 = 0·38, Fig. 1a). As the number of wolves relative to kg of prey increases, the percentage consumed by wolves increases (Table 3). Wolves consumed a greater percentage of their carcasses, the further away they were from the road (Fig. 1b). SWE was also a significant predictor of percentage consumed by wolves. As snow levels increase, wolves consume a smaller percentage of their kills (Fig. 1c). We found that 58% of the variation in percentage consumption could be explained by WPKP, SWE, ROAD and the interaction between SWE and ROAD (Table 3).
Table 3. Regression analyses on the dependent variable, percentage consumed by wolves.* We present results for all significant one variable models and the best overall model
|Independent variables†||d.f.||Coefficient||SE||r2, R2||F-ratio||P-value|
|Constant||55|| 47·7|| 3·54||0·38||33·47||0·0000|
|WPKP|| ||150·2||25·97|| || ||0·0000|
|Constant||55|| 44·4|| 4·55||0·31||25·2||0·0000|
|PACKS|| || 1·19|| 0·24|| || ||0·0000|
|Constant||55|| 55·8|| 3·61||0·16||10·37||0·0000|
|ROAD|| || 0·0076|| 0·0023|| || ||0·0022|
|Constant||55|| 54·8|| 3·54||0·19||13·3||0·0000|
|SWE|| || 4·70|| 1·29|| || ||0·0006|
|Constant||55|| 65·8|| 2·31||0·11|| 6·875||0·0000|
|TMIN|| || −3·21|| 1·22|| || ||0·0113|
|Constant||52|| 29·5|| 4·87||0·58||16·92||0·0000|
|WPKP|| ||103·14||28·1|| || ||0·0006|
|ROAD|| || 0·01|| 0·003|| || ||0·0002|
|SWE|| || 6·66|| 1·75|| || ||0·0004|
|SWE*ROAD|| || −0·0026|| 0·0011|| || ||0·0188|
Figure 1. Relationship between the percentage of a carcass consumed by wolves and (a) per capita, (b) distance to road and (c) snow water equivalent (SWE, note that larger values of SWE represent milder conditions and thus less snow). Percentages are arcsine transformed (20–90 point scale) so that they no longer represent numbers between 0 and 1.
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The regression model was used to predict the effect of wolves on biomass availability in three consecutive winters, characterized by Gese et al. (1996) as follows: 1990–91 mild and little carcass biomass was available; 1991–92 snow arrived early and higher than normal winter severity resulted in substantially more carcass biomass throughout the winter; 1992–93 late onset of snow and a corresponding pulse of carrion biomass. By adding wolves into the model, the scenario changes considerably. During the mild winter of 1990–91, our model reveals that wolves would have increased the amount of biomass available to scavengers from February to March in the Lamar Valley from an estimated 458 kg spanning 4 weeks to 1524 kg spanning 8 weeks (Fig. 2a– note that data collection did not begin until February that year). During the severe winter of 1991–92, the addition of wolves results in a small increase in carrion biomass overall (4232 kg up to 5724 kg from November to March in the Lamar Valley –Fig. 2b) with a decrease in mid-winter carrion when conditions were most severe and a small increase in carrion at the beginning and end of winter when conditions were milder. In the winter of 1992–93, characterized by a late onset of carcass biomass, wolves would have increased the variance of carrion by providing more biomass at the beginning of winter when weather was relatively mild and possibly less biomass at the end of winter when weather was more severe and elk were significantly weakened (2910 kg spanning 13 weeks up to 4468 kg spanning 20 weeks from November to March in the Lamar Valley, Fig. 2c).
Figure 2. Comparison of biomass available in the Lamar Valley, Yellowstone National Park with and without wolves. Light grey bars represent carcass biomass without wolves as measured by Gese et al. (1996). Dark grey bars represent carcass biomass with wolves as derived from our regression model (see Methods). Arrow indicates when data collection by Gese et al. (1996) began. The standard deviation of monthly carrion availability for each of the three years with and without wolves was as follows: (a) 8 vs. 61 kg month−1, (b) 38 vs. 137 kg month−1 and (c) 47 vs. 171 kg month−1.
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As wolf pack size changes, the amount of biomass available to scavengers also changes. Initially the amount of biomass available to scavengers should increase as wolf numbers increase and kill more but eventually should start to decline as wolf numbers increase and wolves consume a higher percentage of their kills. In Fig. 3 (dark circles) we have plotted the relationship between wolf pack size and the total amount of biomass that would have been available to scavengers from one wolf pack in winter 1992–93. The curve reveals that wolf packs of intermediate size provide the most carcass biomass to scavengers. The peak of the curve is most likely skewed towards high wolf pack sizes, however. We used estimates of kg wolf−1 day−1 derived from Smith et al. (2003) which were reported independent of pack size. As wolf pack size increases, however, kg wolf−1 day−1 is likely to decrease. We also plotted the curve (Fig. 3) assuming that kill rate per wolf is a decreasing function of pack size to explore how this would affect the relationship.
Figure 3. Carcass biomass available to scavengers for increasing wolf pack size. Circles represent estimates using data from Smith et al. (2003). Pluses represent estimates assuming a declining kill rate as wolf pack size increases.
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Elk carrion is an important winter food resource for many scavenger species in Yellowstone National Park (Houston 1978). By partially consuming their prey, wolves subsidize scavengers with a high calorie resource that may be essential for metabolic maintenance, growth and/or reproductive success (see Crabtree & Sheldon 1999b for coyotes). In addition, wolves change the timing of the resource from a pulsed resource at the end of severe winters to a more constant resource throughout the winter. This resource subsidy may in turn promote increased biodiversity (Johnson et al. 1996) and lead to larger populations of scavenger species. Female grizzly bears with reliable high-energy foods, for instance, have been shown to attain larger body size and have bigger litter sizes than their counterparts with less reliable and/or lower-calorie foods (Blanchard 1987). Reproduction in magpies, ravens and bald eagles is also highly correlated with the timing and proximity of high-quality food resources (Newton et al. 1982; Swenson, Alt & Eng 1986; Dhindsa & Boag 1990).
Foraging theory provides a context in which to understand and predict the amount of wolf-provisioned carrion biomass available to scavengers. As the difference between the costs and benefits of remaining at a carcass increases, wolves become increasingly likely to abandon the carcass. As a wolf becomes more satiated, the marginal benefit of remaining at a carcass decreases with respect to future calorie gains. Deep snow causes increased energy expenditure in ungulates, resulting in weakened animals that are more vulnerable to predation (Gese et al. 1996). If the next prey item is easier or less risky to attain than guarding the present one, wolves should trade available low-value carcass remains for higher-value organ and large muscle tissue on a fresh carcass that must be obtained at some cost. Costs of remaining increase with proximity of the carcass to the road, while the costs of acquiring the next prey item decrease with increasing snow depth, which is an indicator of prey vigour. Selection for road tolerance may occur in Yellowstone as wolves learn that humans in the park are harmless. This is likely to be balanced by selection against road tolerance outside the park, however, where wolves are sometimes shot or collide with moving vehicles.
Wolf packs of intermediate size provide the largest subsidies to the scavenger guild in YNP. The ratio of the number of wolves to kilograms of prey (WPKP) is the best indicator of how much carrion biomass wolves leave behind to the scavenger guild at a particular carcass. When wolf packs are small, they may not consume much, but their kill rates are low. Conversely, when wolf packs are large, kill rates are high but they also consume a large percentage of their prey. Wolf packs of intermediate size, however, kill at a relatively high rate but consume only part of the carcass, thereby maximizing the subsidy to scavengers.
Gese et al. (1996) found that 54% of the variation in the amount of carcass biomass available to scavengers was due to snow depth and interaction between snow depth and minimum temperature. Our results indicate that, with the reintroduction of wolves, the number of wolves present has become the primary factor determining carcass biomass availability to scavengers with environmental conditions (particularly snow depth) now a secondary factor. From a scavenger's perspective, wolves appear to have changed the source of variance in carcass biomass from one dependent primarily on stochastic, climatic factors to one dependent primarily on a less stochastic, biotic factor – the ratio of wolves to abundance of carcass biomass. The amount of carrion available to scavengers has thus shifted from one dependent primarily on environmental stochasticity to one dependent primarily on wolf demographic stochasticity. Wolves also appear to reduce the variability, within and between years, of carcass availability. Prior to wolf reintroduction, the availability of elk carrion pulsed when severe environmental conditions caused weakened elk to die and ebbed when conditions were mild. Carrion biomass is now less variable during the winter because wolves are killing throughout the year and often partially consuming their kills. In addition, by preying largely on the young and old (Mech et al. 2001), wolves reduce the pool of old, weak animals and so lessen the late winter pulse of carrion when conditions get severe. In other wolf–elk systems, such as Riding Mountain National Park (RMNP) in Canada, natural mortality of elk is rare (Paquet 1992).
We have demonstrated here that wolves mediate the flow of carrion subsidy to scavenger guild members, by controlling the timing and quantity of carcasses. By decreasing the year-to-year variation and increasing the time over which carcasses are available during the winter, this carrion subsidy may contribute significantly to the biodiversity of the region. In RNMP, over 30 species of avian and mammalian scavengers have been documented to use wolf kills (P. Paquet, personal communication). In addition, 57 species of beetles are known to depend on elk carrion in YNP (Sikes 1998). By removing a future meal for wolves, scavengers may in turn cause wolves to kill more often, thus strengthening their top-down effect on vegetation through the control of elk populations. When wolf packs are large or winters are mild, the carrion wolf subsidy will be small. This subsidy increases for wolf packs of intermediate size and as winters become more severe.