Behavioral Ecology Vol. 13 No. 5: 657-663
© 2002 International Society for Behavioral Ecology
Isolation from mammalian predators differentially affects two congeners
Department of Organismic Biology, Ecology, and Evolution, The University of California, 621 Charles E. Young Drive South, Los Angeles, CA 90095-1606, USA Department of Psychology and The Cooperative Research Centre for Conservation and Management of Marsupials, Macquarie University, Sydney NSW 2109, Australia
Address correspondence to D.T. Blumstein, Department of Organismic Biology, Ecology, and Evolution, The University of California, 621 Charles E. Young Drive South, Los Angeles, CA 90095-1606, USA. E-mail: marmots{at}ucla.edu
Received 16 April 2001; revised 10 December 2001; accepted 19 December 2001.
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ABSTRACT |
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Evolutionary isolation from predators can profoundly influence the morphology, physiology, and behavior of prey, but little is known about how species respond to the loss of only some of their predators. We studied antipredator behavior of tammar wallabies (Macropus eugenii) and western gray kangaroos (Macropus fuliginosus) on Kangaroo Island (KI), South Australia, and at Tutanning Nature Reserve on the mainland of western Australia. Both species on KI have been isolated from native mammalian predators for several thousand years. On KI, wallabies (because of their size) are vulnerable to diurnal aerial predators. In contrast, on the mainland both species have been exposed continuously to native and introduced mammalian and avian predators. At both locations, wallabies modified the amount of time they allocated to vigilance and foraging in response to group size, whereas kangaroos did so only at the higher risk Tutanning site. Both species modified overall time budgets (they were warier at the higher risk site), and both species modified space-use patterns as a function of risk. At the higher risk site, tammars were closer to cover, whereas kangaroos were, on average, farther from cover. We hypothesize that the presence of a single predator, even if it is active at a different time of day, may profoundly affect the way a species responds to the loss of other predators by maintaining certain antipredator behaviors. Such an effect of ancestral predators may be expected as long as species encounter some predators.
Key words: group size effects, habitat selection, macropod antipredator behavior, Macropus eugenii, Macropus fuliginosus, relaxed selection, tammar wallabies, time allocation, vigilance, western gray kangaroos.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Studies of populations on predator-free patches of habitat (Magurran et al., 1995
;
Riechert and Hedrick, 1990) or
on predator-free islands (Kavaliers,
1990; Pressley,
1981; Van Damme and Castilla,
1996) and comparisons of species that evolved with and without
certain predators (Coss and Goldthwaite,
1995; Goldthwaite et al.,
1990) illustrate the remarkable variety of morphological,
physiological, and behavioral changes that occur when animals are isolated
from their predators (Magurran,
1999). Although we know that relaxed selection from predators has
myriad effects (Coss, 1999),
previous studies often have focused on the response of a single species to the
loss of a key predator or to the loss of all its predators
(Magurran et al., 1995).
Isolation from all predators is probably a rare event. In this study we
examined two closely related macropod marsupials found sympatrically at two
locations with different evolutionary histories of exposure to predators to
determine how species are differentially affected by the loss of some versus
all of their predators.
The question of how populations respond to the loss of some rather than all
predators has both theoretical and applied importance. Animals live in
environments with multiple predators, yet many studies and models of
antipredator behavior have focused on the effect of a single predator (but see
Bouskila, 1995;
Kotler et al., 1992;
Lima, 1992;
Sih et al., 1998). To better
understand how relaxed selection acts on antipredator behavior, we must
understand how it differentially affects species isolated from some versus all
of their predators. An understanding of these effects has tremendous applied
importance for species now found only on predator-free islands whose historic
range extended onto predator-rich mainlands. In some places, conservationists
translocate or re-introduce insular populations to the mainland
(Johnson et al., 1989). Most
translocations and reintroductions fail
(Griffith et al., 1989;
Wolf et al., 1996), and
predation is often the factor responsible
(McCallum et al., 1995). It
follows that a fundamental understanding of how relaxed selection acts on
antipredator behavior may enlighten conservation efforts.
We focused on two species both found on Kangaroo Island (KI), South
Australia (35°52' S, 136°53' E) and Tutanning Nature
Reserve, a mainland reserve in western Australia (32°32' S,
117°19' E). Tammar wallabies (Macropus eugenii) are
midsized (maximum female mass = 6 kg, maximum male mass = 10 kg), moderately
social, macropodid marsupials. On the mainland they fall prey to both
mammalian and avian predators (Croft,
1989; Smith and Hinds,
1995). In protected areas on Kangaroo Island, wedge-tailed eagles
are the tammar's only predator (Inns,
1980). Western gray kangaroos (Macropus fuliginosus) are
relatively large (maximum female mass = 28 kg, maximum male mass = 54 kg),
social macropodids (Croft,
1989; Poole,
1995). On the mainland, all age classes of kangaroos in their
weight range may be preyed upon by terrestrial mammalian predators (e.g.,
Jarman and Wright, 1993), but
adults face limited risk of predation by aerial predators. In protected areas
on Kangaroo Island, adult kangaroos have little if any exposure to
predators.
Kangaroo Island has been isolated from the Fleurieu Peninsula of South
Australia for about 9500 years (Lampert,
1979). Early European explorers were amazed at the tameness of the
wildlife and attributed it to a lack of predators—including humans
(Peron, 1816). Aboriginal
Australians last occupied Kangaroo Island about 4300 years ago
(Lampert, 1979), and Europeans
primarily colonized the eastern part of the island in the mid-nineteenth
century (Inns, 1980). With the
Europeans came cats (Felis cattus) and farm dogs (Canis
familiaris), which are now found around human settlements. The only
historically important mammalian predator—the Tasmanian devil
(Sarcophilius harrisii)—is known only from the fossil record
(Pledge, 1979). There are no
records of either thylacines (Thylacinus cynocephalus) or dingoes
(Canis lupus dingo) having ever lived on the island. Wedge-tailed
eagles (Aquila audax), a large diurnal raptor, are current residents
(and presumably historical residents) of Kangaroo Island that may prey on
small mammals. Only two smallish owl species live on Kangaroo Island
(Ford, 1979); thus, there is
no risk of nocturnal aerial predation for all but the smallest mammals.
Tutanning Nature Reserve, located in the western Australian wheat-belt, is
a 4000-ha relict forest habitat surrounded by mixed farmland. Tutanning is one
of a few locations where tammar wallabies did not go extinct on the mainland
(Maxwell et al., 1996). The
reserve is also home to western gray kangaroos. A fox baiting program begun in
1996 (Wyre, 1998)
substantially increased the tammar population, and Tutanning has recently
become a source of tammars for translocations to other mainland sites
(Morris et al., 1998). Both
wallabies and kangaroos at Tutanning have consistently been exposed to both
mammalian and avian predators throughout their evolutionary history. Tammars
survived the introduction of dingoes (about 3500 years ago;
Corbett, 1995) and, more
recently, red foxes.
To study antipredator behavior, we examined the time these species
allocated to their most common behaviors, vigilance and foraging. Animals
routinely trade-off antipredatory vigilance against foraging behavior
(Bednekoff and Lima, 1998) and
may become less vigilant if predators are removed or absent
(Berger et al., 1983;
Catterall et al., 1992;
Hunter and Skinner, 1998).
Patterns of time allocation can provide an indication of how animals perceive
predation risk (Bekoff, 1995).
A number of factors are suggested to influence the time animals allocate to
antipredatory vigilance (Elgar,
1989). Two particularly important factors are the distance from
protective cover (Lima, 1987)
and the number of nearby conspecifics
(Coulson, 1999). By comparing
how these factors influence time allocation for wallabies and kangaroos, we
aimed to better understand how antipredator behavior is differentially
influenced by the loss of some versus all of a species' predators.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Subjects and study site
We studied tammar wallabies and western gray kangaroos in Flinders Chase National Park (focusing on animals around the Rocky River ranger station and the Grassdale Conservation Park) on the western end of Kangaroo Island, and in Tutanning Nature Reserve. Both species spend their days in woodland or in dense, impenetrable scrub and emerge around dusk to forage in open meadows. We focused on adult and subadults and collected no data on young-at-foot.
General procedures
We video-recorded 5-min focal animal samples of animals from 1.5 h before
sunset to 4.3 h after sunset on days without heavy rain. We stood or sat in
locations where we had no obvious influence our focal subject's behavior.
Tammars were typically observed between 11 and 50 m, and kangaroos were
typically observed at distances >50 m.
We observed individuals as they moved out of cover to forage. Kangaroos
emerged before tammars; thus some of our kangaroo focals were conducted before
sunset (16/53 on KI; 59/103 at Tutanning), whereas most of our tammar focals
were conducted after sunset (129/141 on KI; 104/104 at Tutanning). After
sunset we affixed image intensifiers (ITT Nightcam 300) with 80-200 mm zoom
camera lenses (Nikkor and Minolta) to the video cameras (Panasonic VX77A). We
illuminated the image-intensified video field with either unfiltered,
red-filtered, or yellow-filtered 1-W headlamps (Petzel). We observed no
difference in the behavior of animals illuminated with the different color
lights, nor did we detect any obvious effect of this temporary low-level
illumination (see also Blumstein et al.,
1999).
Individuals were not captured or marked. Kangaroos were relatively more active at dusk than were tammars, which were primarily active after dark. It was possible to discriminate most individual kangaroos, and some tammars, by day. After dark, individual discrimination was difficult. To avoid observing individuals more than once (i.e., to preserve statistical independence), we systematically walked through the meadows in which animals foraged and did not double-back on our paths. We are confident that most of the observations came from different individuals.
At the beginning of each focal sample, we noted the distance the focal
animal was to protective cover and the group size, defined first as the number
of conspecifics within 10 m and then as the number within 50 m (solitary
animals were scored as being in a group size of one). Group size is one of the
most important variables in explaining variation in wallaby time allocation
(Blumstein et al., in press
b). For macropods, the distance with which conspecifics are scored
as being in a group varies between studies (50 m:
Coulson, 1999;
Heathcote, 1987;
Jarman and Coulson, 1989; 30
m: Hoolihan and Goldizen,
1998; Johnson,
1989; 15 m: Jarman,
1987). We scored group size at two extremes, 10 m and 50 m, and
judged from the animals' behavior how they perceived social companions
(Blumstein et al., 2001).
All distances were measured or estimated from landmarks at known distance
and classified into four categories: 0-1 m, 1-10 m, 10-50 m, and >50 m. We
scored videotaped focals using event-recording software
(Deni, 1996;
Noldus Information Technologies,
1995) and noted the onset of each bout of foraging (included
foraging on the ground and foraging on shrubby vegetation above the ground);
looking while crouching, standing, or while rearing up (a look was scored each
time an individual moved its head and fixated); locomotion, defined as
pentapedal walking (kangaroos and wallabies move their back legs forward while
balancing on their forepaws and tail) and hopping; grooming; affiliative
behavior (sniffing); and aggressive behavior (displacements). We also noted
when animals went out of sight and when they came back into sight. From the
video record, we calculated the proportion of time allocated to each behavior
as a function of the total time an animal was in sight. These analyses focus
on the two most common behaviors, foraging and looking.
In the most commonly used habitat, grassland, we walked 50-m line transects
and recorded the percent groundcover in 1.5-m diam circular plots and
vegetation height (categorized as < 10 m or 
10 m). At KI, we walked 4
lines through grassland leading to 44 plots. At Tutanning, we walked 16 lines
through grassland, leading to 176 plots.
Statistical analyses
We used the individual and values based on aggregation of individuals as
the unit of analysis. Statistical analyses were conducted using StatView 5.0
(SAS Institute, 1998) and
Super-Anova (Abacus Concepts,
1991).
In the subset of data for which age and sex were known, we used Mann-Whitney U tests to test for age and sex effects on time allocation. We also used Mann-Whitney U tests to compare estimates of percent cover and vegetation height in grassland, the most common microhabitat, between sites.
We fitted general linear models to explain variation in the time allocated to vigilance and foraging. We included four main effects: species, site, group size (defined as the number of conspecifics within 10 m), and distance to cover. We included all two-way, three-way, and four-way interactions; the results of some are more important to understand than others. For instance, the three-way interaction of group size x species x site provides a multivariate test of the hypothesis that group size effects are similar for the two species at the two sites. These initial models significantly explained variation in both variables, but we performed a backward-stepping algorithm to maximize the adjusted R2 value (which initially increased after the removal of nonsignificant variables). The least significant variable was removed until the adjusted R2 value began to decline, and we interpret these final models.
To study group size effects in more detail, we aggregated our set of focal
observations to obtain the best possible estimate of the group-size effect at
each group size (defined as the number of conspecifics within 10 m or 50 m).
Antipredator models of vigilance and foraging group size effects predict a
nonlinear relationship between group size and time allocation. Linear
relationships between group size and time allocation may reflect intraspecific
interference competition for limited resources modifying the nonlinear
relationship and would illustrate a fundamental cost of sociality
(Blumstein et al., 2001). We
therefore regressed our aggregated group size against time allocation and
fitted two models to these data: a logarithmic nonlinear model and a linear
model.
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RESULTS |
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The final data set included focal observations where the subject was in sight for
2 min. Analyses are based on a total of 243 observations on
tammars (140 at KI: 21 adult females, 15 adult males, 2 subadult females, 1
subadult male, 92 adults, 9 subadults; 103 at Tutanning: 15 adult females, 12
adult males, 49 adults, 7 subadults, 20 unidentified), and 155 observations on
kangaroos (53 at KI: 21 adult females, 11 adult males, 1 subadult female, 2
subadult males, 18 unidentified; 102 at Tutanning: 36 adult females, 20 adult
males, 10 subadult males, 15 unsexed adults, 6 unsexed subadults, 15
unidentified). For the subset of available data, neither age nor sex significantly explained variation in time allocated to foraging or vigilance (foraging: age, all p > .208; sex, all p > .07; vigilance: age, all p > .148; sex, all p > .063).
There were differences in both potential food and in visibility in the
grassland microhabitat where almost all focal observations were conducted.
Tutanning grasslands had an average of 9% more groundcover than KI (p
= .010). KI grasslands had significantly less tall vegetation ( 10 cm)
than Tutanning (Fisher's Exact test, p = .029).
For clarity, we report the results for vigilance; unless otherwise noted, foraging shows a reciprocal pattern. All main effects were significant (Table 1). Tammars were less vigilant than kangaroos. Animals at Tutanning were more vigilant than at KI (Figure 1). Animals were more vigilant when they were within 1 m of cover compared to farther away. Overall, vigilance decreased with group size.
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Some two-way interactions were significant (Table 1). For species x site interactions, kangaroos increased vigilance more than did tammars between Tutanning and KI. For group size x species interactions, both species showed vigilance group-size effects, but the slope is steeper for tammars. In contrast, for foraging, tammars, but not kangaroos, showed a significant group-size effect. For group size x site interactions, animals on Tutanning had steeper group-size effects than those on KI. Regarding group size x distance-to-cover interactions, there were significant group-size effects at 2-10 m and 11-50 m but not at < 1 m and > 50 m.
Some three-way interactions were significant (Table 1). The key three-way interaction of group size x species x site was significant: Tammars at Tutanning had steeper group-size effects than tammars at KI. Kangaroos at Tutanning had a significant group size effect but not at KI. For group size x distance to cover x species interactions, linear regressions of group size x time allocated to vigilance are only significant for tammars at 2-10 m and for kangaroos at 11-50 m. Small sample sizes prevented any other meaningful analysis. For group size x distance to cover x site interactions, there were no group-size effects on KI at any distance to cover while at Tutanning, there are significant group-size effects at all distances except 0-1 m from cover.
The four-way interaction of group size x distance to cover x species x site was significant (Table 1). There was a significant regression of group size for tammars at Tutanning when they were 2-10 m from cover. For kangaroos (again at Tutanning only), the distance was 11-50 m. Insufficient data prevented us from drawing any conclusions about the pattern < 10 m from cover.
At the higher risk Tutanning site (Figure 2), tammars foraged significantly closer to cover (means; Tutanning = 12 m, KI = 22 m, Mann-Whitney p = .02), while kangaroos foraged farther from cover (means; Tutanning = 83 m, KI = 27 m, Mann-Whitney p < .001).
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The species perceived group-mates differently. For tammars, at both sites, more variation in the time allocated to vigilance and foraging was explained by the number of conspecifics within 10 m than within 50 m (Figure 3; KI: vigilance [log], adjusted R2 = .93, p = .001 at 10 m vs. R2 = 0, p = .54 at 50 m; foraging [linear], adjusted R2 = .93, p = .001 at 10 m vs. a R2 = .18, p = .07 at 50 m; Tutanning: vigilance [log], adjusted R2 = .58, p = .02 at 10 m vs. R2 = .14, p = .16 at 50 m; foraging [log], adjusted R2 = .42, p = .05 at 10 m vs. R2 = .18, p = .13 at 50 m). In contrast, the number of conspecifics within 50 m explained more variation in kangaroo group-size effects, although a significant group-size effect was only found at Tutanning (Figure 3; Tutanning: vigilance [linear], adjusted R2 = .52, p = .03 at 10 m vs. R2 = .53, p = .02 at 50 m; foraging [linear], adjusted R2 = .44, p = .04 at 10 m vs. R2 = .47, p = .03 at 50 m).
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Tammars modified the time allocated to vigilance and foraging as a function of group size at both the lower-risk KI site and the higher risk Tutanning site (Figure 3). In contrast, western gray kangaroos only exhibited statistically significant group-size effects at the higher risk Tutanning site (Figure 3). When present, kangaroo group-size effects were linear; in contrast, nonlinear regression models explained more variation than linear regression models for most tammar group size effects.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Both tammar wallabies and western gray kangaroos modified how they allocated time to behavior in ways that suggest they were sensitive to the risk of predation. They modified their time budgets so that they were warier at the higher risk Tutanning site, and they foraged at different distances from cover. Tammars appeared to perceive cover as protective; they foraged closer to cover at the higher risk site. In fact, tammars routinely return to cover when alarmed. In contrast, gray kangaroos seemed to view cover as obstructive; they foraged farther from cover at the higher risk site. At Tutanning, kangaroos emerging from cover looked around briefly and then hopped to the center of the meadows, where they began foraging.
Two caveats must be made. First, like many other studies of geographic variation in behavior, our "treatments" are not replicated. These were the only two locations where we could study both tammar wallabies and Western gray kangaroos. We have gained statistical power by restricting our studies to these two locations where both species lived. Strictly, our conclusions are limited to these two model species in these two locations. We also must point out that these results may be influenced by the significantly different amounts of groundcover and/or the relative amount of deep vegetation at the two sites. We were unable to test specifically how these variables influenced time allocation because we did not record these at the points where subjects were observed foraging.
In the multivariate models, many terms explained significant variation in time allocation, but the key three-way interaction of group size x species x site reveals that group-size effects varied for the different species and at the different sites. Although we do not have specific data on the relative rates of predation at the sites, we do know about the presence of predators at the sites, and we can make inferences about the presence of predators in the past. We suggest that it is the different histories of predation that are responsible for the different patterns of group-size effects seen in kangaroos and wallabies. Tammars had significant group size effects at both sites, whereas kangaroos had group-size effects only at the higher risk site.
Group-size effects were found in some (Blumstein, unpublished observations;
Coulson, 1999;
Jarman, 1987), but not all
(Colagross and Cockburn, 1993;
Johnson, 1989), previous
studies of macropodid time allocation, but it is possible that some studies
which failed to detect group-size effects used an inappropriate (from the
animal's perspective) distance to define a social group. For instance, Coulson
(1999) used 50 m and found
group-size effects in red-necked wallabies (M. rufogriseus), whereas
Johnson (1989) used 30 m and
did not find group-size effects.
The degree to which antipredator behavior requires experience, and hence
its phenotypic plasticity, varies. Behaviors such as time allocation and space
use seem to be relatively plastic: They varied for both species at both sites
and hence are likely to rely on experience (see also
Hunter and Skinner, 1998). In
contrast, the degree to which cover was obstructive or protective, and whether
or not group-size effects were detected, are seemingly more constrained and
thus are less likely to rely on experience. Why might tammar group-size
effects persist under relaxed selection?
The "ghost of predators past" hypothesis (e.g.,
Byers, 1997; Peckarsky and
Penton, 1988) predicts that tammars have not lost their antipredator behavior
because they were historically subjected to intense predation. Before the
Pleistocene extinctions, mainland Australia had a rich predator community of
thylacinids (marsupial lions/tigers) and dasyurids (quolls, tiger cats, and
devils) (Archer, 1981;
Robertshaw and Harden, 1989).
Although this may explain the persistence of complex antipredator behavior in
some species subjected to relatively relaxed predation pressure since the
Pleistocene extinctions (e.g., Byers,
1997), other species subjected to a history of predation may lose
the ability to recognize predators eliminated by humans in the past century
(e.g., Berger, 1998). Whether a
species quickly loses antipredator behavior following relaxed selection
depends in part on the degree to which behavior is experience dependent (i.e.,
learned or "innate") and, ultimately, on its cost.
The ghost hypothesis assumes that there are no substantial costs to
maintaining antipredator behavior. Tammars may gain other benefits from
aggregating. For instance, rates of affiliative behavior increase with group
size (Blumstein et al., 1999),
and if kin aggregate and engage in beneficial behavior
(Blumstein et al., in press a),
then group-size effects may be maintained by their net benefit.
Lima (1992) modeled the
effects of multiple predators on vigilance behavior in prey and discovered
that one or more relatively innocuous and/or rare predators can have a
substantial impact on prey vigilance. He concluded that more attention should
be paid to the combined effects of predators on prey, a point echoed by others
(Magurran, 1999). Previous
studies assumed that the antipredator behavior we see occurs when predators
are potentially active. Our results suggest that relatively sophisticated
antipredator behavior can be maintained during times when there is no risk of
predation (e.g., eagles do not hunt after sunset).
Coss (1999) noted that
evolutionary persistence of antipredator behavior is expected for functionally
integrated activities. Underlying physiological mechanisms for responding to
predators and managing predation risk may be shared regardless of predator
type (e.g., Blanchard et al.,
1989,
1990). At a genetic level,
pleiotropy will prevent or slow the rate of the loss of formerly adaptive
traits (Byers, 1997) such as
nocturnal antipredator behavior. We hypothesize that the presence of predators
by day will help maintain antipredator behavior at night because it may be a
factor that selects for maintaining integrated antipredator systems. Although
this hypothesis needs a more detailed evaluation, we should note that without
substantial costs for their maintenance, these mechanisms may be sufficient to
explain evolutionary persistence of antipredator behavior in tammar
wallabies.
Wildlife managers planning translocations should pay particular attention
to the history of predation in their source population. Fortunately, our
results suggest that some antipredator behavior (group-size effects) may
persist despite isolation from some predators, while others (space use and
wariness) appear flexible enough for animals to learn themselves
(Hunter and Skinner, 1998)
upon release.
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ACKNOWLEDGEMENTS |
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We thank Des Cooper and Bob Inns for advice on Kangaroo Island tammars; Robert Ellis and the staff at Flinders Chase National Park for hospitality and advice on where to find tammars in the park; the University of Adelaide for access to their biology field station; The Western Australia Department of Conservation and Land Management for permission to work in Tutanning; Les and Cindy Marshall for housing and hospitality while working at Tutanning; Ian McLean for general logistical support in Western Australia; Chris Evans for access to facilities at Macquarie University; Helena Bender, Amos Bouskila, Graeme Coulson, Chris, Andrea Griffin, and Ian for recent discussions about antipredator behavior; and Chris, Andrea, John Byers, Ron Ydenberg, and two helpful anonymous reviewers for comments on previous versions of the paper. Fieldwork was supported by grants to D.T.B. by the Australian Research Council (APD and Small Grant), the Australian Government Cooperative Research Programme, and by Macquarie University (MURG funds). Research protocols were approved by the South Australian Animal Care and Ethics Committee (approval #23/98) and the Macquarie University Animal Ethics Committee (approval #99018), and permits to work with wildlife were issued by the Government of South Australia (license #57) and the Western Australian Department of Conservation and Land Management (license #SF3005).
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