BEHAVIORAL AND ECOLOGIC EFFECTS OF DIFFERENTIAL PREDATION PRESSURE ON MOOSE IN ALASKA Author(s): Kevin S. White, J. Ward Testa, Joel Berger Source: Journal of Mammalogy, 82(2):422-429. 2001. Published By: American Society of Mammalogists DOI: 10.1644/1545-1542(2001)082<0422:BAEEOD>2.0.CO;2 URL: http://www.bioone.org/doi/full/10.1644/1545-1542%282001%29082%3C0422%3ABAEEOD %3E2.0.CO%3B2
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Journal of Mammalogy, 82(2):422–429, 2001
BEHAVIORAL AND ECOLOGIC EFFECTS OF DIFFERENTIAL PREDATION PRESSURE ON MOOSE IN ALASKA KEVIN S. WHITE,* J. WARD TESTA,
AND
JOEL BERGER
Department of Environmental and Resource Sciences, University of Nevada Reno, 1000 Valley Road, Reno, NV 89512 (KSW) Alaska Department of Fish and Game, Division of Wildlife Conservation, 333 Raspberry Road, Anchorage, AK 99518 (KSW, JWT) Program in Ecology, Evolution and Conservation Biology, University of Nevada Reno, 1000 Valley Road, Reno, NV 89512 and Wildlife Conservation Society, P.O. Box 340, Moose, WY 83012 (JB)
We studied behavioral and ecologic effects of differential predation pressure on moose (Alces alces gigas) in the eastern Talkeetna Mountains, Alaska, during 1996–1998. Annual mortality from grizzly bear (Ursus arctos) and wolf (Canis lupus) predation was higher for solitary yearling moose than for dependent yearlings (those with adults) and solitary adults. We tested hypotheses that solitary yearlings have heightened levels of vigilance and greater variation in vigilance responses and spend more time near protective cover than do dependent yearlings or adults. Proportion of time spent vigilant did not differ between solitary and dependent yearlings, and no differences were found between solitary yearlings and adults. However, variation in vigilance increased with distance to protective cover for yearlings but not for adults. Only at distances $20 m from protective cover did variation in vigilance differ between solitary yearlings and adults. Increased variation in vigilance at distances far from protective cover, locations where putative vulnerability to predators is greatest, may account for increased mortality among solitary yearlings. Mean distance to protective cover was not different between solitary and dependent yearlings or between solitary yearlings and adults. Because hypotheses regarding differences in vigilance and use of protective cover between age and social status categories generally were not supported, other factors may be involved in promoting high vulnerability of independent yearlings to predation. Smaller body size and maternal defense are unexplored alternatives for explaining differential mortality between yearlings with and without mothers. Key words:
Alces alces gigas, moose, predation, protective refuge, vigilance
Juvenile mammals tend to be at greater risk of predation than adults (Holmes 1984; Longland and Jenkins 1987; Ross and Jalkotzy 1996). Possible explanations for greater juvenile vulnerability include decreased auditory sensitivity (Lay 1974), smaller size (Lomolino 1984), less experience with their local environment (Longland and Jenkins 1987), delayed detection of potential threats, and longer escape times
(Holmes 1984). Whether behavioral, ecologic, or morphologic in origin, support for these explanations may differ with respect to life-history characteristics that vary across taxonomic groups. Among altricial species, maternal investment plays an important role in juvenile survival (Byers 1997; Caro 1994). Although many studies have focused on active predator defense of vulnerable neonates (Caro 1994; Murie 1981; Owen-Smith 1988), maternal benefits also may extend to
* Correspondent: kevinpwhite@fishgame.state.ak.us 422
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offspring even after they have become relatively independent (Byers 1997; Caro 1994). Mothers can provide social and ecologic information through which offspring derive survival and fitness benefits (Byers 1997), including information relevant to predator recognition and avoidance (Caro 1994). Young also may derive antipredator benefits simply from association with other individuals (Lima and Dill 1990), especially if they are more experienced (Mateo and Holmes 1997). Consequently, naive juveniles may experience considerable antipredator benefits if they associate with older, more experienced individuals, including mothers. Vigilance is an important means by which animals detect, recognize, and avoid predators (Lima and Dill 1990; Quenette 1990). Antipredator responses can be complex. For example, prey animals can exhibit predator-specific behavioral responses (Robinson 1980; Seyfarth and Cheney 1980), and experience seems to be important in development of antipredator responses (Berger 1998; Hunter and Skinner 1998). In general, juveniles tend to exhibit less acute antipredator responses than adults (Arenz and Leger 1997; Seyfarth and Cheney 1980). If younger animals display greater variation in vigilance responses that is independent of mean vigilance rates, then their consequent likelihood of exhibiting inappropriate antipredator responses may increase, resulting in greater mortality than adults. Vigilance behavior is only 1 of several ways in which young animals diminish their chances of predator-associated mortality. They also may base antipredator strategies on ecologic characteristics of their habitat. Where predation risk is high, use of protective cover, or other physical refugia, increases (Berger 1991; Edwards 1983; Kunkel and Pletscher 2000; Molvar and Bowyer 1994). Because risk of predation increases with distance from protective cover, cost of inappropriate antipredator responses also is likely to be greater with in-
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creasing distance from cover (Lima and Dill 1990). We examined questions regarding ecologic and behavioral trade-offs in juvenile moose (Alces alces gigas) with respect to predation. Moose are relatively long-lived and maternal investment in offspring may extend beyond the 1st year of life. Yearlings often associate with mothers after they are capable of social independence. In southcentral Alaska, Testa (in litt.) reported that yearling survival was influenced strongly by association with an adult female, presumably mothers. Solitary, or independent, yearlings were killed by grizzly bears (Ursus arctos) or wolves (Canis lupus) disproportionately more often than were yearlings that were associated with older moose. That variation in mortality, associated with age and maternal association, provides an opportunity to test hypotheses about effects of behavioral and ecologic variables on predator avoidance tactics of socially independent subadult moose. We tested predictions that solitary yearlings are more vigilant, exhibit greater variation in vigilance, and remain closer to protective cover than do yearlings accompanied by mothers. MATERIALS
AND
METHODS
Study area.—Data were collected in the eastern Talkeetna Mountains, Alaska (628N, 1478W). The study area was located in the Oshetna River valley and bounded by the Black River to the north and by the Little Oshetna River to the south, encompassing about 100 km2. Moose densities in that area were considered to be high (0.8 moose/km2) and recruitment was low (Testa and Adams 1998), compared with other northern populations of moose (Boer 1992; Gasaway et al. 1992). Moose typically occurred at elevations of 850–1,060 m in a broad valley bounded to the east and west by steep foothills of the Talkeetna Range. Vegetation was typical of treeline habitats of central Alaska, composed primarily of a mosaic of spruce forest (Picea glauca and P. mariana) and open, brushy tundra dominated by dwarf birch (Betula glandulosa) and willow (Salix sp.—Johnson et al. 1995). Moose in the region were primarily browsers;
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Salix sp. comprised 80–85% of their summer diet in central Alaska (Van Ballenberghe et al. 1989). The Oshetna River valley supported a full complement of natural predators of moose. Densities of grizzly bears (19–23.5 bears/1,000 km2—Miller et al. 1997) and wolves (5.9–9.9 wolves/1,000 km2—J. W. Testa, in litt.) were considered typical of moose ranges throughout south-central Alaska (Gasaway et al. 1992). Annual mortality rates of solitary yearlings were 49% in 1995–1998 (J. W. Testa, in litt.). In contrast, mortality of adult females and yearlings accompanied by mothers was low, annually averaging 5% and 7%, respectively (J. W. Testa, in litt.). Grizzly bear and wolf predation was the principle cause of both adult and yearling mortality (J. W. Testa, in litt.). Alternative prey of grizzly bears and wolves in the Oshetna River valley consisted of caribou (Rangifer tarandus), ground squirrels (Spermophilus sp.), ptarmigan (Lagopus sp.), snowshoe hares (Lepus americanus), and beavers (Castor canadensis). The Nelchina caribou population (between 31,800 and 50,000 in 1996–1998—B. Tobey, in litt.) used the Oshetna River valley for 3–5 weeks in late April to early June during their spring migration (K. S. White, in litt.). Wolves and, to a lesser extent, grizzly bears were the primary predators of caribou in this area (Van Ballenberghe 1985; B. Tobey, in litt.). Sampling.—Data were collected during April– July 1996–1997 and May–June 1998. Focal animal sampling (sensu Altmann 1974) was used to gather data on 26 radiocollared and 45 uncollared adult female and yearling moose using both binoculars and spotting scopes. Yearlings were distinguishable from adults by their smaller size, but in the few cases in which uncertainty existed, no data were gathered. Although association between mothers and yearlings or calves was the predominant association during summer, it is not always possible to be certain that such pairs were related. Nevertheless, we assumed that such affiliations were between mothers and their offspring because adoption in moose seems to be rare (J. W. Testa, in litt.). Unmarked adult females and yearlings were considered independent sampling units if they possessed unique physical characteristics, occurred simultaneously in different locations, were spatially segregated across time, or, for yearlings, observations occurred in different years. Each observation ses-
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sion was subdivided into 180 s and included associated measures of distance to protective cover (m) and duration of vigilance. Those periods subsequently were aggregated into sampling units that comprised observation sessions that were $6 min. This was done to meet assumptions of equal variance for parametric analyses (White 1999). Protective cover was defined as vegetation that was tall and dense enough to conceal a moose from view (Molvar and Bowyer 1994). Distance of the focal animal to cover was estimated visually to the nearest 5 m, using the torso length of a moose (2–2.5 m) as a relative gauge. Periods in which foraging behavior of a focal animal was interrupted by social interactions, elimination behavior, grooming, or resting for .10 s were omitted (Berger et al. 1983). Observation periods were initiated only when animals were feeding. Foraging was defined as biting or chewing of food. A moose was considered vigilant when its head was raised and in an alert posture with ears forward or actively scanning its local environment (Molvar and Bowyer 1994). Measures of vigilance were expressed as the proportion of time vigilant per observation period. Analyses.—Proportional data were arcsine square-root transformed to meet equal variance and normality assumptions of parametric statistics (Neter et al. 1996; Wilkinson et al. 1996). Multifactor analyses of covariance were used to compare the effect of presence or absence of an adult and distance to protective cover on proportion of time vigilant and variation in vigilance (Zar 1999). The latter value was derived by calculating the absolute value of residuals of time spent vigilant. In a separate analysis of covariance, we compared time spent vigilant and variation in vigilance between solitary yearlings and adults, while accounting for the effect of distance to protective cover. A posteriori meancomparison procedures were used to compare differences among categories (Fisher’s least significant difference—Zar 1999). We also used linear regression to examine the relationship between distance to protective cover and time spent vigilant and between distance to protective cover and variation in vigilance. Mean distance to protective cover was compared between solitary adults and independent yearlings and between dependent and independent yearlings us-
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FIG. 1.—Comparison of proportion of time vigilant (arcsine square-root scale) across differing distances to cover between solitary yearling moose (Y 5 0.152 1 0.011X, r2 5 0.29, n 5 14, P 5 0.04) and yearlings accompanied by adults (Y 5 0.237 1 0.003X, r2 5 0.02, n 5 29, P 5 0.46); analysis of covariance r2 5 0.12, F 5 8.278, d.f. 5 3, 39, P , 0.001.
FIG. 2.—Variation (absolute value of residuals) in proportion of time vigilant across differing distances to protective cover between solitary yearling moose (Y 5 0.043 1 0.004X, r2 5 0.35, n 5 12, P 5 0.04) and yearlings accompanied by adults (Y 5 0.072 1 0.002X, r2 5 0.10, n 5 27, P 5 0.11); analysis of covariance r2 5 0.243, F 5 6.50, d.f. 5 3, 26, P , 0.001.
ing nonparametric Mann–Whitney analyses (Zar 1999).
was not supported. Distance to protective cover affected variation in yearling vigilance (F 5 7.24, d.f. 5 1, 35, P 5 0.01), but maternal presence did not (F 5 1.13, d.f. 5 1, 35, P 5 0.30). No interaction occurred between distance to protective cover and maternal presence (F 5 0.55, d.f. 5 1, 35, P 5 0.46; Fig. 2). Nonetheless, variation in vigilance for solitary yearlings increased with distance to protective cover (r2 5 0.35, d.f. 5 12, P 5 0.04), but a significant relationship was not detected among dependent yearlings (r2 5 0.10, d.f. 5 27, P 5 0.11; Fig. 2). If presence of an adult influenced the use of protective cover by yearlings, then solitary yearlings should have been closer to protective cover than dependent yearlings. However, analysis of our data did not reveal such differences (Mann–Whitney U 5 158.00, n1 5 15, n2 5 25, P 5 0.24), even though solitary yearlings tended to occur in closer proximity to protective cover (8.6 m 6 2.8 SE, n 5 15) than dependent yearlings (12.4 6 2.1 m, n 5 25). Solitary yearling and adult antipredator behavior.—Because predation pressure was greater on solitary yearlings than on soli-
RESULTS Maternal presence and yearling antipredator behavior.—If presence of mothers affected yearling vigilance, then independent and dependent yearlings should have differed in their respective responses. That prediction could be tested only after effects of distance to protective cover were accounted for. Distance to protective cover was related to yearling vigilance (F 5 4.95, d.f. 5 1, 39, P 5 0.03), but maternal presence had no effect on vigilance of yearlings (F 5 1.28, d.f. 5 1, 39, P 5 0.27). No interaction occurred between distance to protective cover and presence of an adult (F 5 1.87, d.f. 5 1, 39, P 5 0.18; Fig. 1). Pooling vigilance across all distances to protective cover, mean vigilance was 8.6% (SE 5 2.0, n 5 14) for solitary yearlings and 8.2% (SE 5 1.4, n 5 25) for yearlings with an adult. If maternal presence influenced yearling antipredator behavior, then variation in vigilance should have differed between dependent and solitary yearlings. That prediction
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FIG. 3.—Comparison of proportion of time vigilant across differing distances to protective cover between solitary adult moose (Y 5 0.175 1 0.008X, r2 5 0.33, n 5 19, P 5 0.01) and yearling females (Y 5 0.152 1 0.011X, r2 5 0.29, n 5 14, P 5 0.04); analysis of covariance r2 5 0.305, F 5 12.917, d.f. 5 3, 29, P , 0.001.
tary adults, we expected solitary yearlings to exhibit heightened vigilance relative to adults. Distance to protective cover was related to vigilance (F 5 12.72, d.f. 5 1, 29, P 5 0.001), but age did not affect residual differences in vigilance (F 5 0.11, d.f. 5 1, 29, P 5 0.73). No interaction occurred between age and distance to protective cover (F 5 0.33, d.f. 5 1, 29, P 5 0.572; Fig. 3). Pooling vigilance across all distances to protective cover, the mean was 8.6% (SE 5 1.4, n 5 14) for solitary yearlings and 7.3% (SE 5 1.2, n 5 19) for solitary adults. Accounting for the effect of distance to protective cover, which in that comparison was related only marginally to variation in vigilance (F 5 3.441, d.f. 5 1, 26, P 5 0.075), age did not exert an effect (F 5 0.480, d.f. 5 1, 26, P 5 0.495). However, the interaction between distance to protective cover and age approached significance (F 5 3.949, d.f. 5 1, 26, P 5 0.058), suggesting that variation in vigilance differed with respect to moose age across differing distances to protective cover. Further, variation in yearling vigilance was correlated positively with increasing distance to protective cover (r2 5 0.35, d.f. 5 12, P 5 0.04), whereas variation in adult vigilance was not (r2 5
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FIG. 4.—Variation (absolute value of residuals) in proportion of time vigilant across differing distances to protective cover between solitary adult moose (Y 5 0.060 2 0.000X, r2 5 0.001, n 5 18, P 5 0.92) and yearling females (Y 5 0.043 1 0.004X, r2 5 0.35, n 5 12, P 5 0.04); analysis of covariance r2 5 0.243, F 5 6.50, d.f. 5 3, 27, P , 0.001.
0.001, d.f. 5 18, P 5 0.92; Fig. 4). When distances were .20 m from protective cover, yearling vigilance was more variable than that of adults (Fisher’s LSD, P 5 0.04). Given that solitary yearlings experience greater predation than do solitary adults, we predicted that the former would occur closer to protective cover. However, no differences were found in mean distance to protective cover with respect to age (Mann– Whitney U 5 207.00, nadult 5 23, nyearling 5 15, P 5 0.30). Mean distance to protective cover was 8.6 m (SE 5 2.6, n 5 15) for solitary yearlings and 10.3 m (SE 5 2.1, n 5 23) for solitary adults. DISCUSSION Although optimality theory suggests that antipredator vigilance should be sensitive to increases in predation risk (Berger 1998; Hunter and Skinner 1998; Lima and Dill 1990), we found no support for this supposition. In our study, solitary yearlings were not more vigilant than individuals who were at lower risk of predation. Nevertheless, solitary yearlings showed the greatest variability in vigilance. Variation
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TABLE 1.—Summarya of documented interactions between moose and large carnivores (wolves and grizzly bears) with special emphasis on the type of antipredator response and its subsequent result (proportional values are in parentheses). Wolves b
Interactions Defend Defend–fled Fled Total
No predation 14 15 40 69
(0.87) (0.94) (0.93) (0.92)
Grizzly bears Predation 2 1 3 6
(0.13) (0.06) (0.07) (0.08)
No predation 12 0 3 15
(0.92) (0.00) (0.75) (0.88)
Predation 1 0 1 2
(0.08) (0.00) (0.25) (0.12)
a Sources: Mech 1966; Mech et al. 1998; Murie 1944, 1961, 1981; Nelson and Mech 1993; Peterson 1995; Stephenson and Van Ballenberghe 1995. b Defend 5 interactions that involved active defense (includes charges, stationary defense, and kicking); fled 5 interactions in which moose ran or slowly moved away from the predator; defend—fled 5 interactions involving active defense and escape behaviors.
was related positively to distance to protective cover for yearlings, but not for solitary adults. When $20 m from protective cover, locations where vulnerability to predation was assumed to be greatest, variation in vigilance was higher for solitary yearlings than for adults. Dependent yearlings tended to exhibit variation in vigilance that was intermediate between solitary yearlings and adults. This suggests that association with mothers has a modulating effect on vigilance responses of dependent yearlings and offers indirect support for the contention that yearling vigilance responses may be learned from mothers. Proximate mechanisms explaining increased variation in solitary yearling vigilance could be attributed to either increased interindividual variation or, perhaps, greater intraindividual variation. If variation in solitary yearling vigilance is due to increased interindividual variation, then the resulting increased likelihood of exhibiting inappropriate (particularly low) vigilance responses would be expected to result in greater predation for particular solitary yearlings. Such suboptimal vigilance responses could be due to a variety of factors including poor physical condition, behavioral naiveté, or experience (or lack of) with predators. Conversely, increased intraindividual temporal variation could be an effective response to increased predation. This could occur if increased intraindividual variation is correlat-
ed positively with the complexity of vigilance–feeding sequences. Assuming all other factors are equal, by increasing the complexity, or unpredictability, of vigilance responses, solitary yearlings may reduce the efficiency of stalking predators such as grizzly bears that are reliant on their ability to predict prey behavior to make a successful attack. Further, use of unpredictable behavioral strategies has been suggested for birth-site selection of Alaskan moose and may be a strategy used to reduce predator efficiency (Bowyer et al. 1999). In fact, increased variation in solitary yearling vigilance may be an adaptive antipredator response; however, other factors influencing vulnerability of solitary yearlings to predation (i.e., small body size, lack of maternal association) may reduce efficacy of this behavior. Body-size variation may be an important factor influencing differential vulnerability of juveniles to predation, as suggested for feral horses (Equis caballus—Berger 1986; Turner et al. 1992), black rhinoceros (Diceros bicornis—Brain et al. 1999), and small mammals (Longland and Jenkins 1987). In moose, yearlings are considerably smaller than adults and may lack physical attributes or experience necessary to prevent predator attacks. Adult moose, on the other hand, present a formidable challenge to predators. In 92 documented direct confrontations with grizzly bears and wolves,
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adult moose successfully thwarted predation 88–92% of the time (Table 1). Because only solitary yearlings were especially susceptible to predation in this study, dependent yearlings may derive survival benefits through maternal association—a hypothesis that requires further investigation. With regard to relationships between use of protective cover and predation pressure for yearling and adult moose, neither age nor maternal presence were important determinants of habitat use for moose. Although solitary yearlings tended to spend more time in close proximity to protective cover than solitary adults or dependent yearlings, these differences were not significant. These results do not support the prediction that more vulnerable individuals increase their use of protective cover, or physical refugia, to reduce vulnerability to predation. Although such a relationship has been reported in ungulates (Berger 1991; Edwards 1983; Festa-Bianchet 1988; Kunkel and Pletscher 2000), the foci of such studies were on adults and not young animals. If solitary yearling moose do not respond effectively to the risk of predation by altering habitat use, foraging incentives possibly are more important in determining habitat use than risk of predation. Because of the need to support growth and maintenance, subadult animals experience heightened energetic and nutrient demands compared with nonparous adults, which must only satisfy foraging demands associated with maintenance (Bachman 1993). Increased competition, and perhaps lower forage availability or quality, in ‘‘safe’’ forested areas also may require yearlings to spend more time in areas outside of protective cover than would otherwise be expected. Nevertheless, spatial relationships involving yearlings and adults, presumably mothers, influence vulnerability of yearlings to predation, and variation in vigilance seems to be an important correlate of risk of predation for solitary yearlings, especially when at distances far from protective cover. Although factors relating to body
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size and maternal defense have obvious implications with respect to yearling vulnerability to predation, our results suggested that behavioral patterns also may play an important role in understanding proximate mechanisms that account for increased predator mortality of independent yearlings. ACKNOWLEDGMENTS We wish to thank M. McMurray, D. Spaeth, and J. P. Han for exceptional assistance in collecting field data. W. Longland, G. Hoelzer, and 2 anonymous reviewers provided constructive comments on the manuscript. D. Palmquist provided statistical advice. This study was funded by the Wildlife Conservation Society, Sigma Xi, College of Agriculture at the University of Nevada Reno, Safari Club International, and the National Science Foundation.
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