Mammals - Escape decisions prior to pursuit - Escape and refuge use: theory and findings for major taxonomic groups - ESCAPING FROM PREDATORS: An Integrative View of Escape Decisions(2015)

ESCAPING FROM PREDATORS An Integrative View of Escape Decisions (2015)

Part II Escape and refuge use: theory and findings for major taxonomic groups

IIb Escape decisions prior to pursuit

3 Mammals

Theodore Stankowich and Eigil Reimers

Still prettier were the little oribi. These are grass antelopes frequenting much the same places as the duiker and stein buck and not much larger. Where the grass was long they would lie close with neck flat along the ground and dart off when nearly stepped on with a pig like rush like that of a reedbuck or duiker in similar thick cover. But where the grass was short and especially where it was burned they did not trust to lying down and hiding on the contrary in such places they were conspicuous little creatures and trusted to their speed and alert vigilance for their safety. They run very fast with great bounds and when they stand usually at a hundred and fifty or two hundred yards they face the hunter the forward thrown ears being the most noticeable thing about them. We found that each oribi bagged cost us an unpleasantly large number of cartridges.

Theodore Roosevelt (1910)

3.1 Introduction

Very early in the formal study of mammalogy, scientists began describing “flight distances” estimated in the field, mainly in response to human approachers. Most were observational estimations of the distance at which big game animals fled from hunters, but some provided nuanced descriptions. In the quotation above, Roosevelt (1910), knowingly or not, tells the reader that escape behavior in oribis (Ourebia ourebi) is contextual: when they are afforded concealing vegetation, oribi adopt a strategy of crypsis with very short flight distances, and when they are encountered in more exposed environments, they take flight at much greater distances. In one of the first “comparative” studies of flight behavior, Swiss ethologist Heini Hediger (1964) compiled a list of examples of flight distances of various mammals, birds, reptiles, fish, and invertebrates; most of these entries were one-off observational statements of flight initiation distance (FID) in each species, but others compared FID in different contexts. For example, Kearton (1929) reported that giraffe (Giraffa camelopardalis) flee at 150 yards (135 m) from a man on foot but at only 25 yards (23 m) from a motor-car; Darling (1937) observed that red deer (Cervus elaphus) fled at 50 to 100 yards (46 to 91 m) when being fed but at 600 yards (549 m) when irritable. These and other early reports (Hone 1934; McMillan 1954; Denniston 1956; Altmann 1958; Estes & Goddard 1967) were obviously less rigorous than the hypothesis-driven, structured studies of today that incorporate strict approach protocols and statistical analyses, but they set the foundation for using escape responses as a proxy for animal stress and fear.

Seminal work by Fritz Walther (1969) on the escape behavior of Thomson’s Gazelle (Eudorcas thomsonii) examined escape variation in response to variation in many different factors, including predator species, human activity, temperature, time of day, number of predators, and predator speed. This significant increase in rigor spawned a variety of similar studies in other ungulate species (as well as birds) throughout the 1970s and 1980s (reviewed in Stankowich 2008). By the 1980s, the first formal theories of escape behavior began to develop (Ydenberg & Dill 1986). Studies of escape responses in animals have become more and more commonplace, and we know animals pay attention to a wide variety of factors when deciding when to flee (Stankowich & Blumstein 2005). Despite a wealth of studies of the flight responses of birds (Chapter 4) and reptiles (Chapter 5), studies of flight responses in mammals have been historically limited to ungulates, marsupials, and a few sciurid rodents. Given the exhaustive review of the factors influencing flight responses in ungulates by Stankowich (2008), this chapter will not seek to list every study of escape behavior in mammals, but instead will outline the more significant factors influencing escape responses in mammals, what we can learn from them, what has limited inquiry on this topic in mammals, a case study of reindeer and caribou (Rangifer tarandus), and what our future goals should be in the study of mammal escape responses.

3.2 Predators of mammals and options for escape

Perhaps more than for any other group of vertebrates, risk of predation for mammals is largely based on body size: the larger a prey animal is, the fewer potential predators it will have. But the relationship is not strictly directional. Larger mammal prey are often more desirable targets for larger predators because of the greater energetic reward and smaller mammal prey are often better able to employ crypsis to avoid detection or make use of refugia (e.g., burrows, trees). This often leaves mammals of intermediate size (500 g to 10 kg) at greater risk due to the energetic rewards they confer and more limited ability to avoid detection due to small size; these intermediate-sized mammals tend to have lower metabolic rates, limiting their ability to rely on rapid escape, and are more likely to have morphological antipredator defenses (e.g., spines, quills, body armor) (Lovegrove 2001).

The primary predators of mammals are other mammals, birds of prey, snakes, and sharks (in marine environments) and the vast majority of what we know about mammal escape behavior comes from studies of predation by mammalian carnivores and birds of prey. Given their varied modes of locomotion and lifestyles, mammals show tremendous variation in how they flee from predators (Caro 2005): rapid running, jumping, dropping from trees to the ground, fleeing into a burrow or other cover, climbing trees, moving into water, and even flying away. Predator behavior, however, generally varies in two ways: hunting mode and pursuit duration. Many mammalian predators (e.g., felids), owls, and dangerous snakes hunt by stealth and may only successfully capture a prey animal by approaching very closely without being detected (these predators generally cannot sustain prolonged chases); if prey detect these predators within that range where capture is possible, escape likely immediately follows detection. If the predator is detected at a great enough distance where escape is highly likely, they will often simply monitor and possibly alert/harass the predator until it gives up. When models of large stealthy felid predators were exposed to Columbian black-tailed deer (Odocoileus hemionus columbianus) from 15 to 50 m away, they never fled immediately, but instead stayed alert, snorted, foot-stamped, and alarm walked in order to deter further approach by the potential predator and advertise awareness to the predator (Stankowich & Coss 2007b; Stankowich 2010). Note that mountain lions (Puma concolor) typically need to approach to within 5 to 10 m undetected in order to have a chance to capture a deer (Smallwood 1993). In fact, deer were most alarmed when the model was concealed following exposure (Stankowich, pers. observation); similar observations of heightened alarm responses when visual range is limited have been made in reindeer (Rangifer tarandus) groups interacting with humans (Reimers, pers. observations), and white-tailed deer fleeing in forests vs. pastures (O. virginianus) (Lagory 1987). Coursing predators (e.g., canids) and many diurnal birds of prey, on the other hand, can sustain prolonged chases and will initiate attack from longer distances; therefore prey should flee from such predators at greater distances in order to maintain a spatial margin of safety (Cárdenas et al. 2005). Yellow-bellied marmots (Marmota flaviventris) were much more likely to flee from a gray wolf (Canis lupus) model than they were a mountain lion model, which elicited mostly high levels of vigilance (Blumstein et al. 2009).

Mammals show tremendous variation in their escape strategies, but we can generally group them into four main categories: (1) flee at long range soon after detection and recognition; (2) observe the predator, assess the risk it poses, and decide when to flee in a way that optimizes fitness; (3) rely on crypsis until the last possible moment and then flee if necessary; and (4) hold one’s ground and employ defensive strategies or morphologies (e.g., armor, fighting, toxins). These strategies, however, can vary both intraspecifically and interspecifically. Similar to Roosevelt’s oribi observations, spiny mice (Acomys cahirinus) show dichotomous escape initiation strategies: they either flee early at a long distance, or, if an individual is agile enough, remain frozen and potentially cryptic until the last minute, fleeing only when the predator is very close (Ilany & Eilam 2008).

Wild ungulates are most vulnerable during their first few months of life and may suffer substantial calf losses to predators. This selection pressure has led to two different strategies, hiding and following, for neonatal defense or predator avoidance (Lent 1974). Followers, species in which the neonates accompany the mother within minutes or hours after birth, usually have highly developed social systems and inhabit open terrain with a low vegetative profile. Hiders, species in which the young do not accompany the mother for the first weeks of life, remain in seclusion, minimize their activity, and rely on cryptic coloration and a lack of scent glands to avoid predation. They often live in habitats of dense, high vegetation and respond with alarm bradycardia (decrease in heart rate) upon detecting alarm stimuli, e.g., red deer (Cervus elaphus) (Espmark & Langvatn 1979, 1985) and white-tailed deer (Odocoileus virginianus) (Jacobsen 1979). Deer fawns remain cryptic, hiding in vegetation, and only flee when a predator approaches to within a few meters, and mothers with vulnerable fawns nearby may remain motionless in the face of an approaching predator in an attempt to remain undetected. Detailed accounts of mothers defending their young come from early ethological studies of large ungulates fending off would-be or attacking predators (Lent 1974): mule deer, O. hemionus (Hamlin & Schweitzer 1979); white-tailed deer (Smith 1987); elk, Cervus canadensis, and moose, Alces alces (Altmann 1963); and pronghorn Antilocapra americana (Marion & Sexton 1979). When confronted with coyotes (Canis latrans), white-tails tend to flee, whereas sympatric mule deer are more likely to bunch together with other individuals and attack the predator (Lingle 2001; Lingle & Wilson 2001). Female mule deer with calves will run to and defend fawns that are being attacked by coyotes, using their powerful forelegs to kick and often injure the attackers. Even species with powerfully effective defenses against predators sometimes just turn and run: striped skunks (Mephitis mephitis) ran from approaching predators in nearly 44% of interactions (Larivière & Messier 1996).

Flocking behavior is widespread among mammals, is most conspicuous among larger herbivores, and is primarily influenced by resource availability and distribution (Matthiopoulos 2003), parasites (biting flies, warble flies, and parasitoids; Mooring et al. 2004), and predator pressure (Hamilton 1971). Flight is generally the response when herds interact with predators or humans. Muskoxen (Ovibos moschatus) and African savanna elephants (Loxodonta africana) are exceptions insomuch as their fluid fission-fusion social group system provides a cooperative defense of calves against predators(Lent 1991; Reynolds 1993; Archie et al. 2006).

3.3 Scanning for predators, risk assessment, and flight initiation distance

Prior to encounters with predators, mammals periodically scan their surroundings for potential threats that might be looming. This vigilance may be shared by members of a group, which would likely be more proficient at scanning than a solitary animal that must divide its time between scanning and other activities (e.g., foraging). There is a large literature suggesting that the distance at which a predator begins its approach toward an animal (starting distance: SD) and the distance at which the prey shows overt alertness to that predator (alert distance: AD) are usually strongly correlated with FID (Blumstein 2003; Stankowich & Blumstein 2005; Stankowich & Coss 2006). Theory suggests that the farther away a predator begins its approach and the farther away an animal becomes alert, the longer the distance at which the prey will flee: an animal does better by fleeing earlier to avoid further opportunity costs of staying and maintaining a larger margin of safety (Blumstein 2010; Cooper & Blumstein 2014).

The relationships between SD, AD, and FID, however, are not necessarily linear. Blumstein (2003) found that the relationship between SD and FID was logarithmic in some birds and linear in others, and Blumstein and Daniel (2005) found a strong effect of SD on FID in a comparative analysis of macropodid marsupials. Stankowich and Coss (2006) proposed that the relationship between SD and FID might be logarithmic or even quadratic due to suboptimal scanning rates by prey. If a predator begins its approach from well outside the zone of awareness of a prey (the maximum range at which a prey animal can detect or cares to attend to a predator) the predator may be able to approach closer to the prey before being detected (resulting in a lower FID) relative to an approach where the predator lingers at the edge of the zone of awareness prior to approach and may be detected earlier (Figure 3.1).

Figure 3.1

Predicted relationship between flight initiation distance (FID) and starting distance (SD), where Dmin is the minimum distance at which prey might assess a predator before fleeing and Dmax is the maximum distance at which prey can either detect predators or consider them threatening enough to attend to.To avoid opportunity costs, prey should flee at greater distance when they detect the predator at greater distances. When a predator starts from well outside the prey’s zone of awareness (Dmin-Dmax), it might be able to approach more closely before detection due to suboptimal scanning (α2). Some animals may also be more reactive than others and have a higher Dmax(dashed curve).

(Stankowich & Coss 2006)

Due to suboptimal scanning (variation in α in Figure 3.1: prey cannot detect every predator that enters their zone of awareness the instant that the predator enters it), approaches with longer SD may have shorter FID than those with an SD at the limits of the zone of awareness. Finally, there is often tremendous individual variation in fearfulness or boldness within a population, with some more fearful animals likely having larger zones of awareness than others (Figure 3.1: dashed curve). Stankowich and Coss (2006) approached black-tailed deer from very long distances away, measuring SD, AD, and FID in order to test these hypotheses, and found that a quadratic model provided the best fit to the data (Figure 3.2a).

Figure 3.2

Scatterplots showing relationships between starting distance, alert distance, flight initiation distance, and assessment time of Columbian black-tailed deer in response to a human approacher. (a) Starting distance vs. flight initiation distance: black circles indicate deer that were not alert prior to approach (logarithmic model fit with thin black line), open triangles indicated deer that were alert prior to approach (logistic model fit with dashed line), thick black line indicates overall quadratic model fit (compare to Figure 3.1). (b) Alert distance vs. starting distance; thick curve is a cubic model fit suggesting that deer became alert later when approaches started from outside the zone of awareness. (c) Alert distance vs. flight initiation distance; thick curve is a logarithmic model showing that flight initiation distance increases with alert distance but levels off at Dmax. (d) Alert distance vs. assessment time; deer that became alert earlier assessed the approacher for longer periods (there was no correlation between assessment time and flight initiation distance.

(Stankowich & Coss 2006)

Animals that may have been more fearful of humans (those that were alert prior to approach) had greater FIDs, resulting in a logarithmic model providing the best fit and suggesting that they have a wider zone of awareness, as predicted. This suboptimal scanning hypothesis was further bolstered by the finding that the relationship between SD and AD was also non-linear, with the greatest SDs leading to somewhat shorter ADs than those trials where the approach began at the limits of the zone of awareness (Figure 3.2b). This suggests that the human was able to approach closer to the deer without being detected when he approached from greater distances. Finally, Stankowich and Coss (2006) found a logarithmic relationship between AD and FID (Figure 3.2c): when deer became alert at very great distances, they typically did not flee immediately, instead waiting until the approacher came within 60 to 100 m before taking flight. This finding strengthens the argument that prey assess the threat posed by an approaching predator prior to flight in order to avoid potentially unnecessary and costly bouts of flight; when prey become alert at greater distances they have the luxury of assessing the threat for longer periods of time compared to when detection occurs at a very short distance (Figure 3.2d). Further analyses revealed effects of this pre-flight risk assessment on subsequent escape behavior (e.g., distance fled (DF), escape angle, running style) (Stankowich & Coss 2007a).

3.4 Factors influencing escape decisions in mammals

A huge number of biotic and abiotic factors are known to influence escape decisions in animals (Stankowich & Blumstein 2005) and most of these have been shown in some form in mammals. Stankowich (2008) provided a comprehensive review of escape behavior in ungulates and how it relates to conservation and management; therefore we will not perform a similar review here. Instead we will focus on some of the more important factors for mammals and then examine a case study of escape behavior in reindeer and caribou (Rangifer spp.) because a significant amount of research has been conducted in this system on flight decisions.

3.4.1 Effects of the environment and distance to refuge

Several non-predatory factors in the environment can affect escape decisions in mammals. Mammals appear to be very sensitive to small spatial variation in risk of capture in different environments. Stankowich (2008) found greater escape responses in ungulates in open environments compared to more densely vegetated areas; although some studies didn’t find such an effect. Habitat cover also shortens FID in red kangaroos (Macropus rufus) and euros (M. robustus erubescens) (Wolf & Croft 2010) and brown bears (Ursus arctos) (Moen et al. 2012). In barren habitats one would expect that mammals that are unable to escape underground would seek higher country to improve visual control. Running upslope was the most common response in reindeer when disturbed (Baskin & Skogland 1997; Colman et al. 2001). For example, Reimers found that reindeer groups more often fled uphill (59%) compared to flat (20%) and downhill (21%) flight paths. (E. Reimers, unpublished data). The same data set shows that smell is an important sense for environmental control: the reindeer groups fled into headwind more often (51%) than crosswind (26%) or tailwind (23%). Wolves (Canis lupus) fled at shorter distances in stronger winds (Karlsson et al. 2007). Similar to other taxa (Stankowich & Blumstein 2005), many mammal species have been found to flee at greater distance when they are farther from refuge compared to when there is refuge nearby: woodchucks (Marmota monax; Bonenfant & Kramer 1996; Kramer & Bonenfant 1997), Eastern gray squirrels (Sciurus carolinensis; Dill & Houtman 1989), and degus (Octodon degus; Lagos et al. 2009); Stafl (2013) found no such effect in the American pika (Ochotona princeps).

Insect harassment has been shown to have profound effects on mammal behavior and morphology. For example recent evidence suggests that zebra stripes were favored by natural selection in environments with oppressive activity of biting flies for much of the year (Caro et al. 2014). Insect harassment may have even a greater effect on escape behavior in large mammals than both human infrastructure and predators. During the brief growing season in Arctic and high-mountain ecosystems, undisturbed grazing is crucial in order for reindeer to maximize growth and fattening. In particular warble flies (Hypoderma tarandi) and nose bot flies (Cephenemyia trompe; hereafter referred to as oestrid flies) influence Rangifer behavior (Mörschel & Klein 1997; Anderson et al. 2001; Hagemoen & Reimers 2002) and may amplify or decrease response thresholds in relation to human and predator activities. Throughout warm summers, reindeer are exposed to vigorous oestrid fly harassment, which causes dramatic decreases in feeding and lying, and increase in walking, running, and standing (Figure 3.3). Snow patches, marshes, and windy mountain tops were used primarily to avoid oestrid fly harassment and animals may flee long distances to avoid the insects. Even though Rangifer are disturbed by human activities, they can increase their tolerance toward humans if insect harassment is severe, as shown for domesticated reindeer (Skarin et al. 2004) and caribou observed within the Prudhoe Bay oil field (Pollard et al. 1996). Oil-field gravel pads and roads were used as insect relief habitats (Murphy & Curatolo 1987; Pollard et al. 1996), as animals frequently occupy and take advantage of the shade of buildings and pipelines.

Figure 3.3

Activity budgets (means) of reindeer from scan sampling in relation to oestrid fly harassment in Norefjell and Rondane wild reindeer areas inNorway in 1997. (0 = none, 1 = light, 2 = moderate, 3 = severe.)

(Hagemoen & Reimers 2002)

3.4.2 Habituation to human disturbances and hunting

The vast majority of studies of the effects of human density and traffic on mammal escape behavior have shown that mammals are able to habituate to humans in their environment. Populations in areas with less exposure to humans (smaller populations, less vehicle traffic) have greater FIDs than populations with more exposure to humans, and this finding is robust across different mammalian taxa: ungulates (McMillan 1954; Denniston 1956; Walther 1969; Rowe-Rowe 1974; Tyler 1991; Cassirer et al. 1992; Recarte et al. 1998; Colman et al. 2001; Bekoff & Gese 2003), marmots (Louis & Le Beere 2000; Griffin et al. 2007; Li et al. 2011), and squirrels (McCleery 2009; Chapman et al.2012). There may be, however, a sampling bias such that investigators have preferentially focused their research on species that habituate easily to humans due to ease of access. In fact, some studies have found no habituation effect (Alados & Escos 1988; Lehrer et al. 2011), and some mammals (especially predatory species) are known to not habituate well to humans. However, Wam et al. (2014) recorded a high level of individual plasticity in behavioral responses by protected, re-introduced wolves in Norway toward humans, suggesting that habituation to humans may occur over a longer period of time.

In a meta-analysis of ten studies, Stankowich (2008) found that populations of ungulates under hunting pressure had significantly greater flight responses than non-hunted populations, and more evidence from giraffes (Marealle et al. 2010) and reindeer (Baskin & Hjalten 2001) has supported this finding. The tendency to habituate in ungulates is so strong that the dis-habituating effects of seasonal hunting may not be strong enough to overcome the habituating effects of non-consumptive human exposure (e.g., recreationists) during the rest of the year (Reimers et al. 2009), and the interests of both hunters and wildlife watchers may be satisfied if a balance is struck between these practices.

3.4.3 Type of disturbance

The type of disturbance, be it anthropogenic or a non-human predator, has a significant impact on flight decisions in mammals. Stankowich (2008) found humans on foot to elicit stronger reactions from ungulates (meta-analysis of 11 studies) compared to other types of anthropogenic disturbance (e.g., automobiles, military noise, bicycles, snowmobiles), but sometimes very large machines can be more evocative than pedestrians. Gray (1973) observed muskoxen to respond more strongly to aircraft than to humans, and harbor seals (Phoca vitulina) showed greater AD and FID to boats compared to pedestrians (Andersen et al. 2012). Past experience with such vehicles as a result of being chased by snow machines, helicopters, or fixed wing aircrafts (accidentally or for tagging or other purposes) can rapidly increase alertness and escape behavior. When humans have been a historical source of predation or disturbance, mammals clearly treat them as more dangerous than less threatening human transports (e.g., automobiles, bicycles), but the much greater size of some transports might override this effect and may engender greater fear than single humans on foot, similar to studies from other taxa indicating greater flight responses to larger rather than smaller predators (Stankowich & Blumstein 2005).

Different types of animal predators may also engender greater responses than others according to the relative predation risk they pose. Humans typically evoke a response greater than or equal to the response to domestic dogs (Hone 1934; Hamr 1988; Kloppers et al. 2005) and wolves (Bergerud 1974), but free-ranging dogs remain a significant source of disturbance and stress for wild mammals (Weston & Stankowich 2014). Reindeer had greater AD, FID, and DF in response to a human disguised as a polar bear (Ursus maritimus) than to a human in dark hiking gear (see case study). Finally, Thomson’s gazelles (Eudorcas thomsonii) varied their FID dynamically in response to different species of mammalian predator. Wild dogs (Lycaon pictus) evoked the greatest FIDs, followed by cheetahs (Acinonyx jubatus), lions (Panthera leo), hyenas (Crocuta crocuta), and finally jackals (Canis mesomelas); this order closely agrees with the relative risk posed by each species to the gazelles (Table 3.1; Walther 1969). Jackals rarely ever attack adults and really are only dangerous to fawns. Hyenas kill more fawns than adults but packs of hyenas are far more dangerous to adults than solitary hyenas, resulting in significantly greater FIDs in response to hyena packs relative to solitary individuals. Gazelles flee from lions between 50 and 300 m, a comfortable distance given that lions will kill adults but prefer larger ungulates if they are available. Gazelles show mortal fear of wild dogs and cheetahs, which prefer to hunt gazelles, and to which they responded at the greatest distances (Walther 1969). Mammals clearly assess risk dynamically in response to the threat posed by different types of disturbances and predators, and the types of experiences individuals have with those predators also greatly influences flight decisions (Stankowich & Blumstein 2005; Stankowich 2008).

Table 3.1 Flight initiation distances from different mammalian predators by Thomson’s gazelles (expressed as percentage of cases).

Predator

5-50 m

51-100 m

101-300 m

301-500 m

501-1000 m

>1000 m

N

Jackal

85

15

_

_

_

_

66

Hyena

29

50

10

4

6

1

155

Lion

3

28

62

5

2

_

71

Cheetah

1

3

57

22

15

2

88

Wild dog

_

4

13

20

48

15

44

3.4.4 Effects of group size

Temporary or permanent aggregations commonly formed by mammals have a variety of potential benefits (enhanced vigilance, greater ability to find food or mates, group defense, etc.) and potential costs (easier to locate by predators, potential for disease transmission, interference effects during foraging, social agonism). Declining individual vigilance efforts with increasing group size has been widely reported for both mammals and birds (Elgar 1989; Lima 1995). Wild reindeer in Norway and also on Svalbard adhere to this effect (Reimers et al. 2011, .2012). The effects of group size on escape decisions in mammals, however, have been far less predictable. Stankowich and Blumstein (2005) found a positive effect of group size on FID in terrestrial organisms, but Stankowich (2008) found only a weak, non-robust positive effect (r = 0.13; k = 21 studies) in a meta-analysis on ungulates where heterogeneity among studies was enormous (I2 = 96%). Some studies showed large positive effects (Stankowich & Coss 2007a), while others showed strong negative effects (Matson et al. 2005). Wild reindeer in Norway conform to the latter strategy, FID and DF decreased with increasing group size (Reimers et al. 2012), but the insular wild reindeer of Svalbard have lost their group size effect (Colman et al. 2001; Reimers et al. 2011). Costly antipredator behavior such as these group size effects should not persist on islands once there is no net benefit (Blumstein & Daniel 2005). And indeed, the traditional grouping behavior that characterizes Rangifer elsewhere is absent in Svalbard, where animals live individually or in small groups. High vigilance rates will in most cases compromise feeding time, as suggested by (Laundre et al. 2001). The low scan frequency and total scan duration found in reindeer should not compromise feeding efficiency in any of the study herds. This intraspecific variation in the direction and effect size of group size on escape decisions suggests that group size effects likely interact with the history of the population, reproductive state of the group members, lethality and intensity of human exposure, or openness of the landscape to permit the benefits of collective vigilance (Stankowich 2008).

3.4.5 Effects of insularity and loss of predators

Many studies have shown that local extinction of predators for prolonged periods relaxes natural selection on predator recognition. Over hundreds or thousands of years, prey may lose the ability to recognize locally extinct predators as dangerous (Coss 1999; Berger et al. 2001; Blumstein & Daniel 2005; Blumstein 2006; Stankowich & Coss 2007b; Lahti et al. 2009). Tests of the effects of relaxed selection on escape behavior in mammals are more limited. For instance, Blumstein found that tammar wallabies (Macropus eugenii) living on predator-free islands allowed humans to approach much nearer than tammars living on mainland Australia (Blumstein 2002). In a broader comparative analysis of FIDs in macropodid marsupials, while insularity influenced foraging and vigilance behaviors, living on islands and loss of predators did not have significant effects on escape decisions (see group size discussion above; Blumstein & Daniel 2005), suggesting that effects of relaxed selection may vary between species or be more specifically correlated with time elapsed since isolation. Insular Svalbard reindeer and Greenland caribou show similar effects on foraging and escape decisions (see group size effects above and case study below). Generally, FID may be highly dependent on the individual experiences with predators and humans (Blumstein & Daniel 2005), and one significant traumatic event may be enough to restore recognition of, and responsiveness to, a previously absent predator (Berger et al. 2001).

3.4.6 Social and reproductive effects

Reproductive status influences the escape decisions of both sexes, but a paucity of studies limits our ability to make strong inferences. During times of peak mating (e.g., the rut in ungulates), males typically experience increased costs of fleeing (Ydenberg & Dill 1986) as it may mean abandoning an attractive high-quality territory or even a group of defendable females. This effect has been shown most convincingly in fish and lizards (Shallenberger 1970; Cooper 1997, 1999; Martín & López 1999), but less evidence exists for mammals. Moose and reindeer in rut are much more tolerant of an approaching human than they are just before the rut or when in velvet (Altmann 1958; Reimers et al. 2012), and territorial gazelles flee at shorter distances than solitary bachelors (Walther 1969). Rowe-Rowe (1974), however, found no effect of the rut on flight decisions in blesbok (Damaliscus dorcas). Similar effects of the costs of fleeing occur when individuals are forced to leave a profitable food patch: socially forging degus (Octodon degus) fled at shorter distances in food-rich patches, compared to patches with less food.

Female mammals tend to be warier than males (Stankowich 2008), suggesting that the costs of fleeing are greater for males and/or the benefits of fleeing in the form of protection of nearby offspring and future reproductive potential are greater for females. In fact, many ungulate studies have shown that females with calves flee at much greater distances and flee longer distances than those without calves (Stankowich 2008; Reimers et al. 2011). The presence of pups outside the burrow led to increased AD and FID in Alpine marmots (Marmota marmota) (Louis & Le Beere 2000). Females of some species may even dynamically assess the escape abilities of their young when deciding when to flee from predators: female red kangaroos (Macropus rufus) and female euros (M. robustus) fled at greater distances when they had young at foot compared to those carrying young in their pouch (Wolf & Croft 2010). In sum, both sexes have reproductive considerations during risk assessment, but the different roles that each sex plays in mating and parental investment influences their costs and benefits of fleeing in different ways.

3.4.7 Domestication effects

Price and King (1968) proposed that ‘‘domestication is an evolutionary process involving the genotypic adaptation of animals to the captive environment.’’ There is limited experimental research on the evolution of different traits, including behavior, during domestication. However, there is sufficient evidence based on comparative studies of domestic stocks and their wild ancestors, to identify a number of typical domestication changes, including the following aspects (Jensen 2006): external and internal morphology, physiology, body development, and behavior, which in this context includes reduced fear, increased sociability, and reduced antipredator responses (Price 1997). Interestingly, this complex of changes may develop rapidly, in only a few generations, and in concert, even though only one of the traits is selected for. Belyaev et al. (1985) selected farm foxes only for reduced fearfulness toward humans, and found that the frequency of animals showing this complex of adaptations, including morphological and physiological changes, increased dramatically within 10 to 20 generations. Eurasian reindeer, which are the origin of caribou, may exemplify such complex and rapid adaptations (Reimers et al. 2012, 2014; Nieminen 2013). This subspecies was only recently domesticated by humans, with extensive control of specific herds first evolving during the sixteenth and seventeenth centuries (Mirov 1945). As is demonstrated in the case study, domestication of wild mammals can have significant effects on their escape behavior.

3.5 Case study: reindeer and caribou

3.5.1 Introduction

Reindeer and caribou belong to the same species (Rangifer tarandus), but different subspecies (Banfield 1961). Although the basic behavioral repertoire in the various subspecies appears fundamentally uniform (Thomson 1980), many differences in recorded behavior relate to degree of domestication and to variable factors in the physical and biological environment, herd size and structure, and past experience. While the caribou subspecies are wild, the Fennoscandian tundra reindeer include herds with both wild and domestic origin that vary in number and ecology. The relationship between life history strategies, behavior, and genetics in herds of reindeer that comprise contemporary wild and domestic stocks remains a focal research field. Hunting is the only important wild reindeer mortality factor, because traditional predators, although permanently present or present as stragglers, exert only minor predatory influence. All study herds in Norway are extensively hunted, but molecular genetic analyses (Røed et al. 2008, 2011) shows a clear genetic structure among the study herds that reflect varying degrees of domestic or wild ancestry. The insular Svalbard reindeer is the northernmost population of Rangifer inhabiting an environment without parasitizing insects and, except for a few observations of polar bear (Ursus maritimus) predation (Derocher et al. 2000), no predators (other than man). This situation has prevailed for at least 4000 years (Van der Knaap 1986; Tyler & Øritsland 1989). Unlike Rangifer subspecies elsewhere, Svalbard reindeer live individually or in small groups (Alendal & Byrkjedal 1976), are seasonally sedentary (Tyler & Øritsland 1989), and do not have the nomadic behavior known from other subspecies of Rangifer.

In the absence of four-legged predators, this case study deals with observations of Rangifer behavioral responses primarily to human disturbances in terms of direct provocations by individuals on foot, on ski, or on snowmobile. As a result of extensive field testing in a variety of populations with different degrees of genetic separation from wild reindeer and experiencing different levels of hunting and human recreation exposure, we begin to see how domestication, hunting, and habituation interact to influence escape decisions.

3.5.2 Habituation in relation to genetics, hunting and tourist activities

Assuming domestication selects for and supports tameness, researchers have investigated whether wild reindeer with some domestic ancestry and exposed to hunting remain tame or adopt wild behavior. In the past, restocking of previously wild reindeer habitats has occurred through release of reindeer from domestic herds under the assumption that “a reindeer is a reindeer” and that the introduced animals would eventually adopt behavior similar to wild animals (i.e., redevelop increased vigilance and fear responses). Contrary to expectations, extensive hunting (annual harvest around 30% of the winter herds) since 1956 in Forollhogna, 1967 in Ottadalen, and 1992 in Norefjell has only slightly altered the hard-wired behavioral traits indicative of their history of domestication (Figure 3.4a,b). The frequency of watching the person before flight (Figure 3.5) was 30 to 50% among the wild reindeer herds compared to 80 to 90% among the domestic herds (Reimers et al. 2012). Wild populations on Svalbard show equally weak escape responses, suggesting that factors other than domestication play a larger role in escape responses of Rangifer.

Figure 3.4

(a) Vigilance and (b) escape distances among wild reindeer herds in Norway and in South Georgia and Svalbard. Reindeer of mainly wild origin is denoted W, reindeer with mixed origin WD, and reindeer with domestic origin D. All herds in Norway are hunted on a sustainable basis (attempted kept at a carrying capacity level) while the two hunted herds in Svalbard (Colesdalen and Sassendalen) are subject to light hunting pressure. Hunting was initiated in 1992 in Norefjell and escape data were recorded the summer before hunt (Norefjell I) and again in 2002 to 2006 (Norefjell II). Recreational activities (REC.) are high (H) in Norefjell and Blefjell in Norway and Adventdalen in Svalbard, but moderate (M) in the other areas except in the remote Edgeøya (L) where reindeer rarely are exposed to humans. (X-axis in (b) is broken at 600 m for Rondane and Hardangervidda to allow for a closer inspection of the shorter distances in the other areas. Distance fled is 1722 m in Rondane and 1535 m in Hardangervidda; the SE are maintained in the figure). Recordings of vigilance in South Georgia were made before the eradication of the herd. In a few cases we were able to measure AD but not FID, and FID and not AD. The discrepancies are caused by these unbalanced samples.

(Data from Reimers et al. 2009, 2010, 2011, 2012; Reimers & Eftestøl 2012, and unpublished.)

Figure 3.5

Alerted reindeer males in Ottadalen in May. Antlers in growth and in velvet.

As for the effects of extensive hunting, great differences in vigilance and escape responses persist between the populations despite similar levels of hunting (Figure 3.4). Rondane and Ottadalen are both hunted and experience moderate levels of human exposure, yet reindeer in Rondane show much greater escape responses than those in Ottadalen. Moreover, escape behavior in Norefjell did not change from before hunting was initiated (Norefjell I) after more than ten years of extensive hunting (Norefjell II). Finally, wild reindeer from Svalbard that are subject to light hunting or no hunting show similar vigilance and escape responses to many of the hunted populations of domestic origin in Norway.

As previously discussed, the frequency of encounters with humans may affect ungulate antipredator behavior (see reviews by Stankowich 2008; Tarlow & Blumstein 2007). Although disputed (e.g., Reimers & Colman 2006; Reimers et al. 2007), displacement is the effect most often predicted when recreational activities in wild reindeer are discussed (e.g., Vistnes & Nellemann 2008). While predator pressure is low for all herds, recreational activity has potentially influenced escape responses (Figure 3.4b): recreation and tourism are extensive in Norefjell but moderate in the other areas, and the lower vigilance rate and flight response distances in Norefjell compared to Ottadalen, in spite of comparable domestic origin and extensive hunting, may reflect habituation to the high level of recreational activities in the former. Wild reindeer in Blefjell are exposed to humans more frequently than in Hardangervidda, from which the Blefjell herd originates. The escape response distances (AD, FID, and DF) were shorter in Blefjell than in Hardangervidda, while the probability of assessing the observer before fleeing tended to be greater in Blefjell (Reimers et al. 2010). In Svalbard, Reimers and colleagues (2011) found that vigilance was higher in reindeer in Edgeøya than in the four Spitzbergen areas. Escape responses (AD, FID, and DF) were all shorter in Adventdalen, with its considerably higher amounts of human activities and infrastructure than the other study areas, a finding consistent with habituation toward humans. Greenland caribou escape behavior was similar to that of Svalbard reindeer (Aastrup 2000), reflecting similar histories of the two populations, both having existed for an extended period without large predators and with little hunting interference. Lower probability of assessing before fleeing in Edgeøya (63% vs. 94% in the Nordenskiöld Land areas), along with their higher vigilance, may indicate more frequent interactions with polar bears in Edgeøya in recent years (Reimers & Eftestøl 2012). The overall picture painted by the results in Figure 3.4 suggests that vigilance and escape responses are likely the result of an interaction between genetic origin, exposure to lethal hunting by humans and predators, and non-lethal human recreational activities. Areas lacking predation and having high exposure to humans show very weak escape responses and human recreation has been shown to cause moderate increases in escape responses due to short bursts of seasonal hunting (Stankowich 2008).

3.5.3 Rangifer and predators

Although the literature on Rangifer and their key predators is comprehensive, only two papers (Bøving & Post 1997; Aastrup 2000) address escape behavior and vigilance in caribou to predators. A short publication (Reimers & Eftestøl 2012) includes escape metrics. Female caribou in Alaska foraged in larger groups, displayed a higher rate of vigilance during feeding, and spent less time feeding than did female caribou in West Greenland without predators (Bøving & Post 1997). The results indicate that caribou, like several other species of ungulates, show behavioral adaptations to the risk of predation that are relaxed when this risk is reduced. Svalbard reindeer interact commonly with polar bears. Field work on Edgeøya, Svalbard, measured reindeer response distances from a stalking polar bear, approaches from a person disguised as a polar bear, and “normal” human encounters (Figure 3.4b). Alert and flight initiation distances and distance fled were 1.6, 2.5, and 2.3 times longer, respectively, when Svalbard reindeer were encountered by a person disguised as a polar bear compared to a person in dark hiking gear. Population increase of polar bears on Svalbard and decrease in sea-ice cover in the Arctic region during summer probably results in more frequent interactions with reindeer on the archipelago, indicating a predator-prey relationship between the two species on Edgeøya.

A key prediction of the multipredator hypothesis (Blumstein 2006) is that isolation from all predators may lead to a rapid loss of antipredator behavior, including loss of the group size effect and breakdown of predator recognition abilities. For example, both reindeer and caribou from predator-free regions (Svalbard and West Greenland) were about 3.5 times less vigilant to playback of wolf howling at control sites (Denali National Park and Tetlin Wildlife Refuge) (Berger 2007). Experience-dependent behavior may be lost after the first generation in the absence of predators, while more “hard-wired” antipredator behavior may persist for thousands of years following isolation from predators (Byers 1997; Coss 1999). Domestic reindeer from Norway were introduced to South Georgia in 1911-12 and in 1925 (Leader Williams 1988). After 100 years in absence of predators, vigilance is strongly relaxed (Figure 3.4). On the other hand, experience-dependent behavior may be quickly restored the first time individuals encounter predators (Brown et al. 1997; Aastrup 2000; Berger et al. 2001). In accordance with this, vigilance rates displayed by Svalbard reindeer in Edgeøya, a location with a dense polar bear population, were 2.2 times higher than those of reindeer in Nordenskiöld Land that had fewer polar bears.

3.6 Conservation and management implications

Results from escape behavior studies have strong implications for conservation and management measures in land use planning. Stankowich (2008) makes several suggestions: (1) a broad understanding of how reproductive state and individual biology affects escape decisions is critical for predicting temporal variation in behavior; (2) the interaction between hunting and non-lethal recreation effects may allow consumptive management of populations and still permit convenient wildlife viewing opportunities for ecotourists; (3) knowledge of the extent to which other predators maintain antipredator responses may help predict how wild mammals will respond to human approach; (4) nearby alternative sites may allow wildlife to avoid high levels of human disturbance; and (5) wildlife may respond differently to humans depending on the openness of the environment and distance to potential refugia. Beyond these points, response distances may aid in establishment of buffer zones needed to maintain functional habitats for individual herds (Blumstein & Fernández-Juricic 2010).

3.7 Foci for the future study of mammal escape behavior

The theory and empirical study of escape behavior and risk assessment has been primarily driven by research on birds and reptiles, and, although there is an extensive literature on habituation to human disturbances in large mammals, we know comparatively little about the nuances of mammalian risk assessment. Given the depth of the current literature and the logistical difficulties of working on mammals, we suggest several areas of focus for future work on mammalian escape behavior.

Most studies of escape behavior in mammals examine a single factor or simply test for main effects of several factors. When animals pay attention to multiple factors simultaneously, different factors may interact to create non-additive effects on risk assessment and flight decisions. Some factors may only be important in certain contexts. The effect of distance to the burrow and food abundance only had significant effects on escape responses of degus when they were in social foraging groups, and not when solitary (Vásquez et al. 2002). Interaction effects may be exceedingly important to creating a deeper understanding of the risk assessment process - not just in mammals but in all animals. Potentially interesting interactions for investigation include sex × season, group size × season, and group size × habitat type or distance to refuge.

As previously mentioned, most studies of escape behavior in mammals have focused on ungulates, which tend to be easy to detect from long distance, habituate well to humans (and are thus easy to find), and are often targets of human hunting (making humans more relevant as potential predators). Ungulates are also frequently the focus of key conservation issues in land use conflicts. Broader taxonomic representation is needed, however, to test the same hypotheses regarding the factors influencing risk assessment. Medium-sized to large rodents, marsupials, armadillos, and rabbits could all prove to be tractable research subjects for studies of escape behavior given their visibility and lifestyle.

Similar to Møller’s comparative studies of escape behavior in European and Asian birds (Chapter 4), evolutionary and comparative studies of risk assessment in mammals should be undertaken to understand which factors are most important across taxa and which are more important to individual species with unique ecologies. The taxa mentioned above would be excellent candidates for broad, potentially collaborative, taxon-wide studies of escape behavior using standardized approaches (Chapter 16). These data could also be compared to those from birds and reptiles and other taxa to understand how mammalian ecology influences the factors affecting risk assessment.

3.8 Conclusions

There is a rich history of studying escape behavior in wild mammals. Most of the original observations of flight initiation distance by Hediger (1964) and later workers were made on large, charismatic mammals, primarily to settle conservation conflicts. Nevertheless, while empirical work on flight decisions of birds and reptiles has flourished, similar studies in mammals have been limited primarily to ungulates (Reimers & Colman 2006; Stankowich 2008), for which humans are often a realized predator, and not just hypothetical proxy for a predator. Recent literature on escape behavior of mammals is slowly becoming more taxonomically diverse: brown bears (Moen et al. 2012) and squirrels and marmots (Griffin et al. 2007; McCleery 2009; Lehrer et al. 2011; Li et al. 2011; Chapman et al. 2012). Experience with predators, reproductive effects, and predator hunting behaviors have strong effects on mammalian escape responses. Future efforts should strive to test targeted interactions between factors to understand how species weigh the importance of each factor in different situations. Conducting comparative studies using standard approaches on a wide range of species will also promote an understanding of how morphological traits and ecological variables influence risk assessment.

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