Alarm Calling Upon Predator Detection
KeywordsPrey Species Ground Squirrel Alarm Call Inclusive Fitness Alarm Calling
When a predator is seen, animals from various taxa produce alarm vocalizations. In some cases, alarm calling when a predator is nearby drives the predator away, but in other cases, the caller is pursued by the predator. Calling therefore often leads to greater risk to the vocalizer. Some rodents make anti-predator vocalizations despite this greater threat to themselves because doing so may warn their close relatives of a nearby predator. By warning relatives, they are preserving additional copies of their own genes.
Animal species ranging from birds to mammals are well known to produce alarm calls in response to perceived threats, ranging from unknown and potentially harmful stimuli to known predators. Alarm calls vary in urgency, and some low-arousal calls are produced in response to potential dangers (e.g., an unfamiliar object or animal flying overhead), while others are produced in response to more direct dangers (e.g., a predatory bird swooping from the sky to catch prey species, then perching on a nearby branch) (Bradbury and Vehrencamp 1998). When a prey species produces an alarm call, it can be part of a mobbing response, which involves multiple conspecifics banding together to intimidate a predator and drive it away. Alarm calls can also be produced as part of an escape response, where callers vocalize while fleeing from predators (Zuberbűhler et al. 1997). For both types of alarm calling situation, various hypotheses have been proposed to explain why vocalizing is an adaptive response for prey species and for individual callers within groups of prey species. Calling may drive the predator away, leading to direct benefits to the alarm caller. However, calling may also lead to the alarm caller being targeted by the predator, meaning that other explanations are useful for understanding why this behavior would persist over evolutionary time in prey species (Maynard 1965).
Alarm Caller Targeted by Predator
Animals ranging from birds to mammals make alarm calls when a predator is seen. Such alarm calls are thought to put the vocalizer at risk by attracting the attention of predators. According to theoretical predictions (Hamilton 1964; Dawkins 1976), predators are alerted to a prey individual’s presence and location by their alarm calls, which are often loud and recurrent. In the case of group-living prey animals, predators would more likely pursue a noisy individual over a silent one (Maynard 1965). Animals who vocalize in response to a threat are therefore more likely to be pursued by that predator, according to theoretical biologists (Hamilton 1964; Maynard 1965; Dawkins 1976). Although results are mixed (e.g., Cresswell 1994; Zuberbűhler et al. 1997), evidence from several mammal and bird species supports the idea of callers being targeted by predators. For example, in the American pika (Ochotona princeps), predatory weasels were seen actively pursuing alarm callers immediately following their vocalizations (Ivins and Smith 1983). In Belding’s ground squirrel (Urocitellus beldingi), predators including coyotes and weasels were seen chasing callers following their alarm vocalizations (Sherman 1977). For Gunnison’s prarie dog (Cynomys gunnisoni), individuals did not alarm call if they were in very close proximity to a predator, suggesting increased risk from alarm calling (Hoogland 1996). For bell miner (Manorina melanophrys) bird nestlings, vocalizations of any kind increased risk of consumption by avian or rodent predators (McDonald et al. 2009). In each of these cases, vocalizing is thought to have put the prey individual at greater risk (Sherman 1977). Alarm calling is therefore not an adaptive behavior at proximate level for individuals of these species, meaning it does not enhance their personal survival. Evolutionary explanations are necessary to account for the development and persistence of anti-predator vocalizations in these animals.
Alarm calling is more obviously adaptive for species where vocalizing by an individual directly discourages predatory pursuit (Maynard 1965). Alarm calling in response to a predator’s presence is advantageous if calling drives the predator away, thus decreasing the level of threat to and directly benefiting the individual who calls (Hamilton 1964). The pursuit deterrence hypothesis (Sherman 1977) suggests that alarm calling is adaptive for the caller because it discourages predatory targeting and leads to increased survival for the caller. Vocalizations are therefore directed towards predators rather than nearby conspecifics (Wheeler 2008). Anti-predator vocalizations are the acoustic dimensions to multifaceted mobbing behaviors, which communicate to stealth predators that prey are aware of their presence (Sherman 1977; Bradbury and Vehrencamp 1998). Evidence that acoustic signaling deters an ambush predator from approaching or pursuing prey has been found in a number of taxa, ranging from birds to mammals such as ungulates and primates. For the Eurasian skylark (Alauda arvensis), individuals who sang when chased by predatory falcons were less likely to be caught than animals who remained silent (Cresswell 1994). For the klipspringer antelope (Oreotagrus oreotagrus), alarm calling was thought to signal predator awareness and to discourage pursuit (Tilson and Norton 1981). For primate species including Campbell’s guenon (Cercopithecus campbelli), the sooty mangabey (Cercocebus atys), the Diana monkey (Cercopithecus diana), the lesser white-nosed monkey (Cercopithecus petaurista), the western black and white colobus (Colobus polykomos), and the western red colobus monkey (Colobus badius), stealth predators such as leopards stopped pursuing monkey groups that made alarm calls at high rates (Zuberbűhler et al. 1997). In each of these cases, animals made alarm vocalizations in response to perceived threat, and these calls reduced their own risk of predation by driving predators away at increased rates.
Anti-predator vocalizations are highly variable in their utility to individuals (Bradbury and Vehrencamp 1998). For some species, alarm calls encourage predator pursuit and increase vulnerability to predation (e.g., Ivins and Smith 1983), while for other species, alarm calls drive predators away (e.g., Cresswell 1994). Anti-predator vocalizations are adaptive at proximate level if they directly discourage a predator from pursuing an individual but are not advantageous to the individual if calling encourages predatory pursuit (Maynard 1965; Sherman 1977). Other hypotheses for the evolution of alarm calling should therefore be considered. If alarm calling does not lead to increased survival for the caller, evolutionary explanations involving inclusive fitness, altruism, group selection, and genetic representation in the animal’s social group should also be investigated.
Alarm Callers and Genetic Representation
Prey animals from a broad range of taxa produce alarm calls in response to threats. While in some cases alarm calling has been found to discourage pursuit by stealth predators (e.g., Zuberbűhler et al. 1997), for other species, alarm calling puts the individual who calls at greater risk of pursuit (Maynard 1965; Dawkins 1976; Sherman 1977). For prey species where the latter applies, theoretical models predict that alarm calling would be adaptive for individuals if calling improved the chances of survival for their relatives (Hamilton 1964; Dawkins 1976). How related an alarm caller is to a relative can be determined by the co-efficient of genetic relatedness (r), which quantifies the level of genetic relationship between any two individuals of the same species (Wright 1922; Hamilton 1964). The co-efficient reflects the probability that at any given genetic locus, genes passed down will be identical due to shared ancestry between individuals. Clones or identical twins would have a relatedness co-efficient of r = 1, while unrelated individuals would have a co-efficient close to r = 0. Clones or identical twins would therefore share 100 % of the genes found at specific loci due to inheritance from common ancestors, while unrelated individuals would share no genes found at specific loci due to shared inheritance. Amongst non-clone relatives, individuals are most closely related to their offspring, full siblings, and parents (all r = 0.5) and less closely related to grandparents, aunts/uncles, cousins, and half-siblings (r = 0.25 or less) (Wright 1922).
According to theoretical predictions by Hamilton (1964) and Maynard Smith (1965), individuals are more likely to alarm call, thus putting themselves at greater risk of predation, in situations where doing so benefits their close relatives (i.e., offspring, siblings, and parents) by warning them of a nearby threat. Therefore, individuals would make alarm calls in dangerous situations and put themselves at increased risk because their signaling would lead to increased survival for kin, thus saving copies of the caller’s own genes from predation (Dawkins 1976; Sherman 1977). Evidence supporting this idea has been found for numerous rodent species from the squirrel family (Sciuridae). For example, female Belding’s ground squirrels (Urocitellus beldingi) who had relatives in their group made alarm calls at higher rates than other group members (Sherman 1977, 1981). Similarly, individual Richardson’s ground squirrels (Urocitellus richardsonii) were most likely to alarm call when they had offspring or siblings nearby (Davis 1984). For the Eastern chipmunk (Tamias striatus), adult females called at higher rates when close to relatives, who were likely to live in neighboring burrows (da Silva et al. 2002). In the Alpine marmot (Marmota marmota), adult males who were related to most group members alarm called at higher rates than other individuals (Barash 1976). In the black-tailed prairie dog (Cynomys ludovicianus), individuals alarm called at higher rates when offspring, siblings, or parents lived nearby (Hoogland 1995), while in the Gunnison’s prairie dog (Cynomys gunnisoni) females with nearby kin or offspring made anti-predator calls at the highest rates (Hoogland 1996). Despite these many examples of rodents from the squirrel family, strong evidence for the increased genetic relatedness of vocalizers to nearby conspecifics is lacking for species in other taxa, although other social mammals, such as the tufted capuchin (Cebus apella), have been tested (Wheeler 2008). There is clearly wide variation in how anti-predator alarm calls are functional and adaptive for each animal species. Consideration of the life history of many Sciuridae rodents, where close kin such as parents, offspring, and siblings (all r = 0.5) typically live or are located in close proximity to alarm callers, may help explain why genetic representation significantly affects alarm calling behavior in many species of this taxonomic group. For other animal species, theoretical explanations other than genetic relatedness should be considered in addressing how alarm calling behavior is adaptive.
Although anti-predator vocalizations are used by prey animals across taxonomic groups, there is wide variation in how these vocalizations are employed. Alarm calls attract predator attention and put the vocalizer at increased risk in species including ground squirrels and birds but drive the predator away in prey species including antelope and monkeys (Sherman 1977; Tilson and Norton 1981; Zuberbűhler et al. 1997; McDonald et al. 2009). Different explanations exist addressing why alarm calls are adaptive for each animal species. Alarm calls may function in predator deterrence or may lead to an alarm caller being targeted by a predator (Wheeler 2008). In situations where alarm calling brings additional risk, individuals may call if close kin such as offspring, siblings, or parents are nearby. By warning relatives, alarm callers from the squirrel family are thought to promote the survival of their genes as represented in their kin (Sherman 1977, 1981). However, for other animal taxa, other adaptive explanations should be considered for the persistence of risky alarm calls.
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