UC Davis UC Davis Previously Published Works Title Isolation rearing reveals latent antisnake behavior in California ground squirrels (Otospermophilus becheeyi) searching for predatory threats. Permalink https://escholarship.org/uc/item/3gj370jd Journal Animal cognition, 18(4) ISSN 1435-9448 Authors Tromborg, Chris T Coss, Richard G Publication Date 2015-07-01 DOI 10.1007/s10071-015-0853-5 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Anim Cogn (2015) 18:855–865 DOI 10.1007/s10071-015-0853-5 ORIGINAL PAPER Isolation rearing reveals latent antisnake behavior in California ground squirrels (Otospermophilus becheeyi) searching for predatory threats Chris T. Tromborg • Richard G. Coss Received: 2 September 2014 / Revised: 23 December 2014 / Accepted: 16 February 2015 / Published online: 1 March 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract This study of California ground squirrels Introduction (Otospermophilus beecheyi) investigated the long-term effects of isolation rearing on alarm-call recognition. Six The antipredator behavior of California ground squirrels wild-caught squirrels, trapped as yearlings, and six (Otospermophilus beecheyi), a species that occupies sub- laboratory-reared squirrels were maintained in solitary terranean and terrestrial habitats, has been extensively cages for approximately 3 years prior to the study. Visual studied and described (Hanson and Coss 1997; Owings and searching and olfactory searching were measured as Leger 1980; Owings and Coss 2008). Like other species squirrels emerged from their burrow-like nest box into a (Boinski et al. 2003), their antipredator behavior is often laboratory room after hearing repetitive playbacks of alarm expressed by anticipatory vigilance that can inform them calls or control sounds consisting of pulses of white-noise about the state of their surroundings and can allow them to or ambient laboratory sounds. Before exiting completely differentiate between dangerous and routine situations. after hearing alarm calls, both groups exhibited similar Vigilant behavior is often provoked by conspecific alarm levels of visual searching that was reliably higher than after calls, which are extremely salient and nearly always pro- hearing the other sounds. After exiting completely, the voke physiological arousal and behavioral responses laboratory-reared squirrels exhibited a reliably greater (Owings and Virginia 1978; Owren and Rendall 1997). amount of olfactory investigation than the wild-caught Alarm calls can also act as Pavlovian unconditioned stimuli squirrels. Five laboratory-reared squirrels turned around (Griffin 2004; Lea et al. 2008). The evocative nature of after exiting and inspected their dark nest-box opening, alarm calls may be an outcome of their intensity, structure, three of which tail flagged repeatedly and one threw sub- or temporal patterning (see Morton 1977). The effective- strate into the opening. Since pups recognize snakes and ness of these calls could also reflect their recognizable engage in this behavior, this latent expression of antisnake information-related properties as signals (Rendall and behavior illustrates its robust organizational properties in Owren 2013; Stegmann 2013) or might even suggest the the appropriate burrow-like context irrespective of the presence of innate recognition systems in perceivers presumed retardation of neural development known to (Davies et al. 2004). occur in other species of rodent subjected to similar iso- Antipredator vocalizations have been argued to provide lation rearing. information about external referents, including the type and behavior of predators, the arousal level of the vocalizer, or Keywords California ground squirrels Á Alarm calls Á the location of the perceived threat (Coss et al. 2007; Innate antisnake behavior Á Isolation rearing Á Nest-box Owings and Leger 1980; Seyfarth et al. 1980; Strusaker exiting Á Olfactory investigation Á Visual searching 1967). Such behavior has been observed in California ground squirrels (Owings and Hennessy 1984). The loco- motor and vocal behavior of ground squirrels varies during & C. T. Tromborg Á R. G. Coss ( ) the differently urgent contexts associated with the detection Department of Psychology, University of California, Davis, CA 95616, USA of raptors, mammals, and snakes (Leger and Owings 1978; e-mail: [email protected] Owings and Hennessy 1984; Owings and Virginia 1978). 123 856 Anim Cogn (2015) 18:855–865 Avian predators can appear suddenly and swoop toward a should adopt an elongate posture while keeping the eyes squirrel, allowing little time for escape and eliciting the and noses near the ground for maximum information ac- least deliberative evasive behavior (Fitch et al. 1946; quisition. If a predator is actually detected, a squirrel’s Hanson and Coss 1997). Ground squirrels respond to the head motion should be arrested and the target fixated for detection of a rapidly moving raptor by emitting whistle further assessment (cf. McAdam and Kramer 1998; alarm calls and fleeing indiscriminately toward the nearest Quenette 1990; Treves 2000). cover (Hanson and Coss 1997; Leger et al. 1979). Once Conceptually, an annulus of territory surrounding the detected, stealthily approaching mammalian predators can burrow opening represents a critical region wherein there is be predictable and avoided in an organized manner. a nearly instantaneous transition in the urgency and con- Squirrels detecting a stealthily approaching mammal figuration of predatory contexts as squirrels move between typically assume positions near burrows or on promonto- the subterranean and terrestrial environments (Coss and ries from which they monitor the predator’s movements, Goldthwaite 1995; Coss and Owings 1985; Tromborg often emitting chatter vocalizations (Leger et al. 1979; 1998). The antipredator behavior of ground squirrels can be Owings et al. 1986; Owings and Leger 1980). Ground viewed within two contexts as they emerge from burrows: squirrels can also hear alarm calls from within their bur- a preemergent condition in which vision is more restricted rows. Such alarm-call transmission within burrows has and olfaction and audition predominate in environmental been demonstrated in other fossorial mammals (Heth et al. assessment and a postemergent condition in which, while 1986). Groups of ground squirrels have been observed to vision predominates, all sensory modalities are employed. emerge from their burrows seconds after hearing alarm Preemergent squirrels must maneuver from subterranean calls and to then briefly scan their surroundings. locations where visual cues are absent to terrestrial vantage Throughout a ground squirrel’s ontogeny, antipredator points where vision becomes effective. Postemergent vocalizations are nearly universally provocative. Initially, squirrels can employ these vantage points to assess their their predictive properties appear to be unrefined; these surroundings in order to detect changes that might have vocalizations primarily incite arousal (Mateo 1996a, b). occurred since the previous surveillance period. For ground This activated physiological condition could be a require- squirrels, this type of interruption in the availability of ment for an important course of directed learning to occur information occurs cyclically during their nocturnal re- (Gould and Marler 1987). In ground squirrels, directed tirement into burrows. learning involves the maturation of perceptual processes important in the recognition of predators and in the Experimental questions and predictions execution of antipredator behavior (cf. Mateo 1996a, b; Palleroni et al. 2005; Seyfarth and Cheney 1980). Com- This study investigated the manner in which laboratory- pared with experienced adults, immature California ground reared and wild-caught California ground squirrels differed squirrels venturing above ground are chronically aroused in their responses after hearing alarm calls and control physiologically without any obvious provocation (Hanson sounds in a laboratory setting. Visual searching and ol- and Coss 2001a). As a result, they engage in higher levels factory searching were investigated when squirrels first of undirected environmental assessment. They also exhibit emerged from their nest boxes into a laboratory room distinctly inferior antipredator tactics related to mapping simulating an outdoor setting after an overnight interrup- escape routes on local terrains, are less discriminating than tion in the opportunity to engage in environmental adults about the differing levels of risk posed by avian assessment. We predicted that, after hearing alarm calls, versus mammalian predators, and are less adept at wild-caught ground squirrels would engage in elevated executing appropriate responses to different antipredator levels of visual and olfactory searching upon initial emer- vocalizations (Hanson and Coss 1997; Loughry and gence from their nest boxes, but would reduce this after the McDonough 1989; Mateo 1996a, b). animal had emerged completely. Under the same condi- tions, laboratory-reared squirrels were predicted to be less Risk assessment during burrow emergence discriminating in the response to the sound treatments and engage in lower levels of visual and olfactory searching. The behavioral properties of environmental assessment as manifested by visual searching should reflect the spatial locations from which major predators launch attacks. As Methods with other species, squirrels searching for avian predators