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Vocalization as a social signal in defensive behavior
CHAPTER 5.1
Vocalization as a social signal in defensive behavior Yoav Litvin1*, D. Caroline Blanchard2 and Robert J. Blanchard1 1
Department of Psychology, University of Hawaii at Manoa, Honolulu, HI, USA Pacific Biosciences Research Center, University of Hawaii at Manoa, Department of Genetics and Molecular Biology, John A. Burns School of Medicine, Honolulu, HI, USA
2
Abstract: Impending dangers elicit alarm vocalizations aimed at conspecifics, and these calls in turn elicit defensive responses in recipients. The notion that these vocalizations represent adaptive responses to threat, enhancing the survival and reproduction of potentially-related conspecifics, is supported by findings from laboratory and field studies. These observations show that vocalizations occur predominantly when the vocalizing animal is in the presence of conspecifics (colony); that higher rates may occur in females; that animals may reduce their own risk of negative consequences by calling preferentially from a place of relative safety; and that dominant males, which tend to sire differentially numbers of offspring within a group, may show higher calling rates, reflecting their status-dependent activities within the group and territory. Both laboratory findings in rats and field observations of various social species suggest that alarm vocalizations include emotional and referential or descriptive information with reference to the source of threat and its characteristics. Research into common mechanisms may shed light on the underpinnings of a variety of human psychiatric conditions associated with fear and anxiety. Keywords: defense; conspecific; VBS (visible burrow system); predator; alarm vocalizations; defensive threat; anxiety; fear
I. Defense
of elaborate patterns of species-specific defensive behaviors (Endler, 1997; Dawkins and Krebs, 1979; Blanchard and Blanchard, 2008). In rodents, an extensive repertoire of innate defensive behaviors can be seen in predator–prey interactions in natural and semi-natural (laboratory) situations. To predator threat, rodents of small prey species exhibit a general cessation of ongoing nondefensive activities (e.g., grooming, playing, foraging, feeding and sexual behavior) in both adults (Blanchard and Blanchard, 1989) and preweanling pups (Takahashi, 1992), along with enhancement of avoidance, flight, freezing, risk assessment, defensive threat and defensive attack behaviors (Blanchard and Blanchard, 2008). Rodents will also readily bury novel, aversive, or potentially dangerous objects (Treit et al., 1981). Manifestation of specific behaviors is dependent on a number of factors: (1) context – an
Defensive behaviors constitute a diverse range of responses to immediate and potential threats in the environment (Blanchard and Blanchard, 2008). A defensive repertoire is constructed of such behaviors, each of which has proved successful in response to particular types of threats in particular situations. Natural threats may include dangerous features of the environment, predators and associated cues, and conspecific attack (Endler, 1986). Inanimate environmental threat sources, such as floods or fires, elicit relatively few and simple defenses, whereas interactions with animate threats, such as predators and conspecifics, may involve an intricate arms race that ultimately facilitates the development
*
Corresponding author. E-mail: [email protected]
Stefan M. Brudzynski (Ed.) Handbook of Mammalian Vocalization ISBN 978-0-12-374593-4
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DOI: 10.1016/B978-0-12-374593-4.00015-2 Copyright 2010 Elsevier B.V. All rights reserved.
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animal will typically flee a threat within an environment in which escape is possible, yet when trapped it will freeze; (2) stimulus ambiguity – whereas ambiguous stimuli, such as predator odors, elicit risk assessment behaviors (e.g., stretch attend, stretch approach, olfactory investigation) and are often associated with a state of anxiety, discrete, present threats elicit flight, avoidance, defensive threat and attack, and are associated with a state of fear; (3) defensive distance – the distance between predator and prey shifts defensive coping strategies from avoidance to escape, with short distances to the threat and unavoidable contact culminating in defensive threat and attack postures. In addition to environmental influences on the evolution of defense, organismic factors influence the relative importance of each behavior within a complete repertoire. For example, while practically all vertebrates and many invertebrates show some form of behavioral defense, the metabolic restrictions of cold-blooded reptiles may have promoted a shift toward passive defensive strategies, such as avoidance and hiding, at least in colder climates, whereas the emergence of warm-blooded mammals enabled rapid evolution of active strategies, such as escape and defensive threat and attack (Edmunds, 1974; see also Porges and Lewis, Chapter 7.2 in this volume). Within mammalia, long legs and flight as a predominant defense are interactive features, each promoting the success of the other, particularly for animals living in open plain habitats. In members of gregarious, but not solitary, species it is highly adaptive for animals to develop the ability to both emit and detect signals that may serve as warnings against potential or present dangers.
II. Defensive vocalizations The evolution of intricate social networks in vertebrate animals has been paralleled by the development of communication skills that are also integrated into the defensive repertoires of some avian and many mammalian species, ranging from rodents to primates (Bradbury and Vehrencamp, 1998). Vocal communications of threat are manifested as “alarm vocalizations” (also “alarm calls,” or “alarm cries”) that serve to communicate information about imminent or potential threats in the environment. Alarm vocalizations may carry information about the threat source, such as its intensity and potential attack vector (e.g., terrestrial,
aerial, fossorial), as well as information about the sender such as size, sex, age, or even social status. Mammals integrate defensive vocalizations, which span sonic to ultrasonic ranges, as a response to a variety of adverse circumstances; e.g., when presented with unpleasant or painful stimuli (Kaltwasser, 1991), as a defensive threat (Darwin, 1872), when in danger (Greene and Meagher, 1998; Manser et al., 2002) and immediately following a successful retreat into safety (Blanchard et al., 1991; Blumstein and Armitage, 1997). These different vocalizations usually have different functions when directed at the threat source or at (nonattacking) conspecifics as the target of the communication. Consequently, some ambiguity has arisen as to the precise definition and usage of the term “alarm vocalization” or “alarm cry” (Litvin et al., 2007), either as a warning signal of the presence of danger, targeted toward conspecifics (Maynard Smith, 1965; Sherman, 1977) or as a defensive threat vocalization intended directly to deter an oncoming threat, such as a predator (Fitzgibbon and Fanshawe, 1988; Hasson, 1991; Blumstein, 1999; Swaisgood et al., 1999), or indeed both (Shelley and Blumstein, 2004). These distinctions signify very different causality and functions, but field studies and laboratory observations have demonstrated both types of vocalizations in a variety of animals. An analysis of the differences between alarm vocalizations and defensive threats has been presented elsewhere (Litvin et al., 2007). Here, we refer to “alarm vocalizations” in the context of social signals directed at conspecifics.
II.A. Laboratory studies There are three types of ultrasonic vocalizations (USV) which have been identified and described in laboratory rats (Rattus norvegicus) (Blanchard et al., 1986; Brudzynski et al., 1993). When isolated from the dam, rat pups emit circa 40 kHz short vocalizations; an infant distress call or isolation vocalization (Brudzynski et al., 1999). Juvenile and adult rats produce two kinds of USV; a high-pitched and short, circa 50 kHz USV, and a low-pitched and longer, circa 22 kHz USV. 50 kHz USV are emitted in non-aggressive conspecific social interactions (Blanchard et al., 1993), during play (Knutson et al., 1998), and during male ejaculation (McIntosh and Barfield, 1980). Such calls have also been reported during fighting in male conspecifics (Sales and Pye, 1974; Burgdorf et al., 2008). Furthermore, rats will work for playback of
Vocalization as a social signal in defensive behavior these calls, suggesting that they produce a positively valenced appetitive state. Adult rats emit 22 kHz USV in a variety of situations (for review see Sales and Pye, 1974; Brudzynski, 2005): (1) during the post-ejaculatory period (Barfield and Geyer, 1972; Barfield and Thomas, 1986); (2) in intraspecific defensive/submissive postures in the context of intermale social interactions (Lore et al., 1976; Thomas et al., 1983; Portavella et al., 1993); (3) when in the presence of a predator (Blanchard et al., 1991, 1992); (4) when startled during opiate and cocaine withdrawal (Vivian and Miczek, 1991; Mutschler and Miczek, 1998; Covington and Miczek, 2003); and (5) when subjected to chronic pain (Calvino et al., 1996). In contrast to readily “self-administering” playback of 50 kHz recordings, rats avoid playback of 22 kHz vocalizations, further suggesting that the latter are aversive (Burgdorf et al., 2008). Collectively, these findings indicate that 22 kHz USV are elicited in stressful situations and can be used as indices of aversive affective states (Bell, 1974; Brudzynski, 2001; Knutson et al., 2002). Careful observation and analysis of alarm vocalizations within a laboratory setting has enabled their use as indices of affective states in rats and mice (Bell, 1974; Brudzynski, 2001; Knutson et al., 2002; see also Brudzynski, Chapter 7.3 in this volume) in a variety of both conditioned and unconditioned models of anxiety (Vivian et al., 1994; Brudzynski and Chiu, 1995; Miczek et al., 1995; Sanchez, 2003; Koo et al., 2004; Nunes Mamede Rosa et al., 2005). This laboratory has observed and analyzed alarm vocalizations in the semi-natural context of a visible burrow system (VBS) consisting of an open surface area connected to tunnels and chambers and containing small mixedsex groups of adult rats and sometimes also pups born in the habitat. Following a week of habituation to the context, a cat was introduced into the surface area for 15 minutes and USV were recorded for an additional 175 minutes after removal of the cat. A control/sham procedure 2–3 days later presented a toy cat in the VBS, followed by a second (real) cat exposure after an additional interval of the same length. The resident rats displayed a consistent and highly reliable sequence of behaviors in response to cat exposure. On the first exposure, rats quickly fled into the burrows, subsequently emitting 22 kHz USV (actually 18–24 kHz USV) that lasted for about 30 minutes after the cat was removed and gradually subsided thereafter. Although the dominant male was typically the only rat on the surface and actually in
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visual contact with the cat, a single initial vocalization often recruited additional vocalizations from other members of the group (Blanchard et al., 1991). During cat exposure and for several hours afterward, rats reduced or ceased non-defensive activities such as eating, copulation, or conspecific social interactions while avoiding the surface of the VBS. When presented with the toy cat control, rats also quickly fled into the burrows and emitted 22 kHz USV, yet these behaviors did not persist; they quickly resumed normal non-defensive activities. A second cat exposure produced identical behaviors to the first exposure, including flight, risk assessment and 22 kHz USV, indicating little habituation to cat presentation in the VBS. However, when rats were exposed individually to a cat either in a VBS or an open field cage that provided no escape, they did not produce USV (Blanchard et al., 1991), congruent with the notion that USV are indeed alarm vocalizations oriented towards conspecifics (compare with results obtained in single cages; see Wöhr and Schwarting, Chapter 4.2 in this volume). Playback of 22 kHz USV induced a noticeable reduction in the behavior of the listening rats, further strengthening the notion that these are conspecific alarm calls (Brudzynski and Chiu, 1995). In addition, playback of 22 kHz USV appeared to induce vocalizations from conspecifics as young as 10 days of age when in a social setting (Blanchard, unpublished observations). Rat pups on postnatal day 10 responded to the playback by emitting USV of approximately 27 kHz. These calls were markedly different from the typical 40 kHz isolation calls of young pups separated from the dam. In contrast, separated rat pups on postnatal day 14 inhibit the typical 40 kHz infant distress calls (isolation vocalizations) on encountering a threatening stimulus (adult male conspecific) (Takahashi, 1992). Collectively, these findings suggest that 27 kHz vocalizations serve a different function than 40 kHz pup vocalizations and may be related to the classic 22 kHz alarm vocalizations of adult rats. It is useful to analyze the timing and duration of 22 kHz USV within the complete defensive repertoire displayed in the context of the VBS. On introduction of the cat into the VBS, rats reliably exhibited several types of defenses, with flight closely followed by emission of USV. During the most intense periods of USV emission, rats were most often freezing, but this immobile period invariably involved orientation toward the tunnel leading to the surface area of the VBS, constituting a rather passive form
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of risk assessment. After the USV died down, more active forms of risk assessment gradually appeared, including approach to the openings of the surface area. Rats might extend their heads closer and closer to these openings over time, orienting their eyes and ears to the surface, but without actually entering it (Blanchard and Blanchard, 1989). These observations fit well with an interpretation that circa 22 kHz USV in rats serve to warn colony members of the presence of danger, whereas risk assessment activities enable the subject to assess the likelihood of this danger, initially from a relatively safe location (the tunnel or burrow) and later, in the absence of any further indication of danger, with forays onto the surface itself. Thus, these behaviors, both emission of USV and risk assessment activities, serve as components of a defensive decision-making sequence, with USV promoting defensiveness and risk assessment reducing it (given that, as in these studies, the cat is no longer present). This process provides an indication of the essential conservatism of the defensive process in that the interval between the gradual phasing out of alarm USV in these colonies and the first entry of any rat onto the surface area was about five hours. Better safe than sorry. However, these behaviors did not end the defensive sequence. When the first rat (always the dominant) re-entered the surface area, it would quickly sprint across to the near corner of the open space, exiting one tunnel and entering another in a few seconds or less. Such “corner runs” may be an efficient way to assess the potential danger of a situation further, by soliciting an attack from the no-longer-visible threat source, when such attack is unlikely to be successful because the rat’s period of vulnerability is so short. As such, it may represent an additional form of risk assessment. Sex differences in emission of USV to a live cat included differences in the frequency and duration of emission, as well as in the sonographic characteristics of these calls, with females reliably producing more frequent and longer USV than males. While cat exposure produced high levels of USV in both sexes, perhaps indicative of a ceiling effect (maximal response), potential threats (cat odor alone) produced marked sex differences. Sonographic analyses showed consistent differences in the patterns of USV emitted by the two sexes. Females showed a mean frequency of 22.2 kHz with a narrow frequency distribution, while males showed a mean frequency of 20.1 kHz with a wider distribution, congruent
with the expected relationship between body size and vocalization frequency (see Fletcher, Chapter 3.1 in this volume). Six major subtypes of vocalizations were described based on the sonographic structure: horizontal; linear ascending; linear descending; U-shaped; negatively accelerated ascending; and negatively descending pulses. Females showed higher levels of horizontal, linear descending, U-shaped and negatively accelerated ascending USV, while males largely emitted negatively accelerated descending pulses. These sex differences are in accordance with the notion that in addition to their emotional content, 22 kHz USV carry significant informative value; it may be adaptive for females to produce more USV due to their care of pups, a particularly vulnerable group of conspecifics that may be closely related to the caller. Gender variation in the sonographic characteristics of alarm vocalizations may also provide a valid means of recognition of the caller’s gender or other features. The wide range of USV characteristics that show variation may also contribute to the identification of unique signals through which individual rats may be recognized. Recent studies of responses of rats to olfactory stimuli from cats indicated their ability to discriminate between individuals (Staples et al., 2008). These findings suggest that the complexity of 22 kHz vocalizations may provide a parallel in terms of individual identification of conspecifics.
II.B. Field studies Recent studies of animal communication question the classical distinction between the semantic communication of human language and the emotionrelated calls of animals. Field observations show that threat-linked animal vocalizations may be evaluated in terms of both their informative value, i.e., the reliability with which a call signifies the presence of a threat, and their referential specificity, i.e., the precision with which particular stimuli elicit a specific call type (Seyfarth and Cheney, 2003). The field literature contains many examples of vocalizations oriented toward conspecifics that include referential or descriptive information with reference to the source of threat and its characteristics. African meerkat sentinels (Suricata suricatta) (meerkat groups usually consist of 3 to 30 individuals) cease foraging and climb to high ground or to the tops of shrubs to assess better the danger of possible predator threats (Clutton-Brock et al., 1999). When such a
Vocalization as a social signal in defensive behavior threat is detected, meerkats emit alarm vocalizations that have been shown to convey information regarding both predator type and the urgency of danger to its group (Manser et al., 2002). Vocalizations of black-capped chickadees (Poecile atricapilla) convey predator size to conspecifics, subsequently modulating their defensive reactions (Templeton et al., 2005). Diana monkeys (Cercopithecus diana) produce differential alarm calls for aerial and terrestrial predators, as well as for predators, nonpredators and other general disturbances (Zuberbühler et al., 1997). Belding’s ground squirrels (Spermophilus beldingi) emit alarm calls that have been shown to be nepotistic warnings preferentially directed at relatives (Sherman, 1977); young squirrels learn to respond more quickly to calls signifying fast-moving predators than to those indicative of slow-moving ones, thus demonstrating both their referential value and their importance for survival (Mateo, 1996). Gunnison’s prairie dogs (Cynomys gunnisoni) produce four different types of alarm calls depending on the type of predator, which result in two different responses by conspecifics (Kiriazis and Slobodchikoff, 2006). Several species of marmots (Marmota flaviventris, M. olympus, M. caligata, M. monax) emit alarm calls directed towards pups in order to warn them of danger (Blumstein and Armitage, 1997, 1998; Daniel and Blumstein, 1998). The alarm calls of a number of species are modified by the immediacy of a threat, with distant threats eliciting one type of call and immediate threats a distinctly different call (Klump and Shalter, 1984; Macedonia and Evans, 1993). Similarly, defensive responses of Richardson’s ground squirrels (Spermophilus richardsonii) vary in accordance with the proximity of the conspecific caller, with neighbor squirrel calls eliciting higher levels of vigilance than non-neighbor calls, indirectly indicative of the threat urgency (Hare, 1998). A number of phenomena observed in rat VBS studies are supported by field work with other mammals. The dependence of vocalizations on the presence of conspecifics is in line with observations of similar calls in other rodent species (Blumstein and Armitage, 1997, 1998). Female Belding’s ground squirrels (Sherman, 1977) and marmots (Blumstein and Armitage, 1997, 1998) showed significantly higher alarm vocalizations, akin to findings showing enhanced levels of 22 kHz USV in female rats (Blanchard et al., 1992), observations suggesting greater adaptive value for female alarm calls as their young are more likely to be in close proximity. Meerkats and marmots emit alarm
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vocalizations from a place of relative safety. Similarly, rats in the VBS are more likely to emit USV from within the burrows. Field studies in meerkats (CluttonBrock et al., 1999) and marmots (Blumstein and Armitage, 1997) showed a link between dominance and risk assessment, suggesting that dominant animals are also more likely to produce alarm vocalizations. In the VBS, dominant males are more likely than subordinates to occupy the surface area, and as a result are more likely to first encounter threat-related stimuli, and to initiate alarm vocalizations.
III. Conclusions The study of defensive behaviors and their biology may be relevant to analysis of a number of human emotion-related behaviors. In this context, alarm vocalizations are particularly interesting as they may shed light on the social and communicatory aspects of anxiety and other threat-related emotions. Laboratory and field studies suggest that alarm vocalizations in a variety of species serve to convey both emotion and information related to the caller and the threat source. Their conservation over mammalian species, and in particular their strong association with species showing gregarious social systems, provide substantial support for a view that human alarm or warning vocalizations may provide a strong functional parallel to those of non-human mammals.
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Vocalization as a social signal in defensive behavior Yoav Litvin1*, D. Caroline Blanchard2 and Robert J. Blanchard1 1
Department of Psychology, University of Hawaii at Manoa, Honolulu, HI, USA Pacific Biosciences Research Center, University of Hawaii at Manoa, Department of Genetics and Molecular Biology, John A. Burns School of Medicine, Honolulu, HI, USA
2
Abstract: Impending dangers elicit alarm vocalizations aimed at conspecifics, and these calls in turn elicit defensive responses in recipients. The notion that these vocalizations represent adaptive responses to threat, enhancing the survival and reproduction of potentially-related conspecifics, is supported by findings from laboratory and field studies. These observations show that vocalizations occur predominantly when the vocalizing animal is in the presence of conspecifics (colony); that higher rates may occur in females; that animals may reduce their own risk of negative consequences by calling preferentially from a place of relative safety; and that dominant males, which tend to sire differentially numbers of offspring within a group, may show higher calling rates, reflecting their status-dependent activities within the group and territory. Both laboratory findings in rats and field observations of various social species suggest that alarm vocalizations include emotional and referential or descriptive information with reference to the source of threat and its characteristics. Research into common mechanisms may shed light on the underpinnings of a variety of human psychiatric conditions associated with fear and anxiety. Keywords: defense; conspecific; VBS (visible burrow system); predator; alarm vocalizations; defensive threat; anxiety; fear
I. Defense
of elaborate patterns of species-specific defensive behaviors (Endler, 1997; Dawkins and Krebs, 1979; Blanchard and Blanchard, 2008). In rodents, an extensive repertoire of innate defensive behaviors can be seen in predator–prey interactions in natural and semi-natural (laboratory) situations. To predator threat, rodents of small prey species exhibit a general cessation of ongoing nondefensive activities (e.g., grooming, playing, foraging, feeding and sexual behavior) in both adults (Blanchard and Blanchard, 1989) and preweanling pups (Takahashi, 1992), along with enhancement of avoidance, flight, freezing, risk assessment, defensive threat and defensive attack behaviors (Blanchard and Blanchard, 2008). Rodents will also readily bury novel, aversive, or potentially dangerous objects (Treit et al., 1981). Manifestation of specific behaviors is dependent on a number of factors: (1) context – an
Defensive behaviors constitute a diverse range of responses to immediate and potential threats in the environment (Blanchard and Blanchard, 2008). A defensive repertoire is constructed of such behaviors, each of which has proved successful in response to particular types of threats in particular situations. Natural threats may include dangerous features of the environment, predators and associated cues, and conspecific attack (Endler, 1986). Inanimate environmental threat sources, such as floods or fires, elicit relatively few and simple defenses, whereas interactions with animate threats, such as predators and conspecifics, may involve an intricate arms race that ultimately facilitates the development
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Corresponding author. E-mail: [email protected]
Stefan M. Brudzynski (Ed.) Handbook of Mammalian Vocalization ISBN 978-0-12-374593-4
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DOI: 10.1016/B978-0-12-374593-4.00015-2 Copyright 2010 Elsevier B.V. All rights reserved.
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animal will typically flee a threat within an environment in which escape is possible, yet when trapped it will freeze; (2) stimulus ambiguity – whereas ambiguous stimuli, such as predator odors, elicit risk assessment behaviors (e.g., stretch attend, stretch approach, olfactory investigation) and are often associated with a state of anxiety, discrete, present threats elicit flight, avoidance, defensive threat and attack, and are associated with a state of fear; (3) defensive distance – the distance between predator and prey shifts defensive coping strategies from avoidance to escape, with short distances to the threat and unavoidable contact culminating in defensive threat and attack postures. In addition to environmental influences on the evolution of defense, organismic factors influence the relative importance of each behavior within a complete repertoire. For example, while practically all vertebrates and many invertebrates show some form of behavioral defense, the metabolic restrictions of cold-blooded reptiles may have promoted a shift toward passive defensive strategies, such as avoidance and hiding, at least in colder climates, whereas the emergence of warm-blooded mammals enabled rapid evolution of active strategies, such as escape and defensive threat and attack (Edmunds, 1974; see also Porges and Lewis, Chapter 7.2 in this volume). Within mammalia, long legs and flight as a predominant defense are interactive features, each promoting the success of the other, particularly for animals living in open plain habitats. In members of gregarious, but not solitary, species it is highly adaptive for animals to develop the ability to both emit and detect signals that may serve as warnings against potential or present dangers.
II. Defensive vocalizations The evolution of intricate social networks in vertebrate animals has been paralleled by the development of communication skills that are also integrated into the defensive repertoires of some avian and many mammalian species, ranging from rodents to primates (Bradbury and Vehrencamp, 1998). Vocal communications of threat are manifested as “alarm vocalizations” (also “alarm calls,” or “alarm cries”) that serve to communicate information about imminent or potential threats in the environment. Alarm vocalizations may carry information about the threat source, such as its intensity and potential attack vector (e.g., terrestrial,
aerial, fossorial), as well as information about the sender such as size, sex, age, or even social status. Mammals integrate defensive vocalizations, which span sonic to ultrasonic ranges, as a response to a variety of adverse circumstances; e.g., when presented with unpleasant or painful stimuli (Kaltwasser, 1991), as a defensive threat (Darwin, 1872), when in danger (Greene and Meagher, 1998; Manser et al., 2002) and immediately following a successful retreat into safety (Blanchard et al., 1991; Blumstein and Armitage, 1997). These different vocalizations usually have different functions when directed at the threat source or at (nonattacking) conspecifics as the target of the communication. Consequently, some ambiguity has arisen as to the precise definition and usage of the term “alarm vocalization” or “alarm cry” (Litvin et al., 2007), either as a warning signal of the presence of danger, targeted toward conspecifics (Maynard Smith, 1965; Sherman, 1977) or as a defensive threat vocalization intended directly to deter an oncoming threat, such as a predator (Fitzgibbon and Fanshawe, 1988; Hasson, 1991; Blumstein, 1999; Swaisgood et al., 1999), or indeed both (Shelley and Blumstein, 2004). These distinctions signify very different causality and functions, but field studies and laboratory observations have demonstrated both types of vocalizations in a variety of animals. An analysis of the differences between alarm vocalizations and defensive threats has been presented elsewhere (Litvin et al., 2007). Here, we refer to “alarm vocalizations” in the context of social signals directed at conspecifics.
II.A. Laboratory studies There are three types of ultrasonic vocalizations (USV) which have been identified and described in laboratory rats (Rattus norvegicus) (Blanchard et al., 1986; Brudzynski et al., 1993). When isolated from the dam, rat pups emit circa 40 kHz short vocalizations; an infant distress call or isolation vocalization (Brudzynski et al., 1999). Juvenile and adult rats produce two kinds of USV; a high-pitched and short, circa 50 kHz USV, and a low-pitched and longer, circa 22 kHz USV. 50 kHz USV are emitted in non-aggressive conspecific social interactions (Blanchard et al., 1993), during play (Knutson et al., 1998), and during male ejaculation (McIntosh and Barfield, 1980). Such calls have also been reported during fighting in male conspecifics (Sales and Pye, 1974; Burgdorf et al., 2008). Furthermore, rats will work for playback of
Vocalization as a social signal in defensive behavior these calls, suggesting that they produce a positively valenced appetitive state. Adult rats emit 22 kHz USV in a variety of situations (for review see Sales and Pye, 1974; Brudzynski, 2005): (1) during the post-ejaculatory period (Barfield and Geyer, 1972; Barfield and Thomas, 1986); (2) in intraspecific defensive/submissive postures in the context of intermale social interactions (Lore et al., 1976; Thomas et al., 1983; Portavella et al., 1993); (3) when in the presence of a predator (Blanchard et al., 1991, 1992); (4) when startled during opiate and cocaine withdrawal (Vivian and Miczek, 1991; Mutschler and Miczek, 1998; Covington and Miczek, 2003); and (5) when subjected to chronic pain (Calvino et al., 1996). In contrast to readily “self-administering” playback of 50 kHz recordings, rats avoid playback of 22 kHz vocalizations, further suggesting that the latter are aversive (Burgdorf et al., 2008). Collectively, these findings indicate that 22 kHz USV are elicited in stressful situations and can be used as indices of aversive affective states (Bell, 1974; Brudzynski, 2001; Knutson et al., 2002). Careful observation and analysis of alarm vocalizations within a laboratory setting has enabled their use as indices of affective states in rats and mice (Bell, 1974; Brudzynski, 2001; Knutson et al., 2002; see also Brudzynski, Chapter 7.3 in this volume) in a variety of both conditioned and unconditioned models of anxiety (Vivian et al., 1994; Brudzynski and Chiu, 1995; Miczek et al., 1995; Sanchez, 2003; Koo et al., 2004; Nunes Mamede Rosa et al., 2005). This laboratory has observed and analyzed alarm vocalizations in the semi-natural context of a visible burrow system (VBS) consisting of an open surface area connected to tunnels and chambers and containing small mixedsex groups of adult rats and sometimes also pups born in the habitat. Following a week of habituation to the context, a cat was introduced into the surface area for 15 minutes and USV were recorded for an additional 175 minutes after removal of the cat. A control/sham procedure 2–3 days later presented a toy cat in the VBS, followed by a second (real) cat exposure after an additional interval of the same length. The resident rats displayed a consistent and highly reliable sequence of behaviors in response to cat exposure. On the first exposure, rats quickly fled into the burrows, subsequently emitting 22 kHz USV (actually 18–24 kHz USV) that lasted for about 30 minutes after the cat was removed and gradually subsided thereafter. Although the dominant male was typically the only rat on the surface and actually in
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visual contact with the cat, a single initial vocalization often recruited additional vocalizations from other members of the group (Blanchard et al., 1991). During cat exposure and for several hours afterward, rats reduced or ceased non-defensive activities such as eating, copulation, or conspecific social interactions while avoiding the surface of the VBS. When presented with the toy cat control, rats also quickly fled into the burrows and emitted 22 kHz USV, yet these behaviors did not persist; they quickly resumed normal non-defensive activities. A second cat exposure produced identical behaviors to the first exposure, including flight, risk assessment and 22 kHz USV, indicating little habituation to cat presentation in the VBS. However, when rats were exposed individually to a cat either in a VBS or an open field cage that provided no escape, they did not produce USV (Blanchard et al., 1991), congruent with the notion that USV are indeed alarm vocalizations oriented towards conspecifics (compare with results obtained in single cages; see Wöhr and Schwarting, Chapter 4.2 in this volume). Playback of 22 kHz USV induced a noticeable reduction in the behavior of the listening rats, further strengthening the notion that these are conspecific alarm calls (Brudzynski and Chiu, 1995). In addition, playback of 22 kHz USV appeared to induce vocalizations from conspecifics as young as 10 days of age when in a social setting (Blanchard, unpublished observations). Rat pups on postnatal day 10 responded to the playback by emitting USV of approximately 27 kHz. These calls were markedly different from the typical 40 kHz isolation calls of young pups separated from the dam. In contrast, separated rat pups on postnatal day 14 inhibit the typical 40 kHz infant distress calls (isolation vocalizations) on encountering a threatening stimulus (adult male conspecific) (Takahashi, 1992). Collectively, these findings suggest that 27 kHz vocalizations serve a different function than 40 kHz pup vocalizations and may be related to the classic 22 kHz alarm vocalizations of adult rats. It is useful to analyze the timing and duration of 22 kHz USV within the complete defensive repertoire displayed in the context of the VBS. On introduction of the cat into the VBS, rats reliably exhibited several types of defenses, with flight closely followed by emission of USV. During the most intense periods of USV emission, rats were most often freezing, but this immobile period invariably involved orientation toward the tunnel leading to the surface area of the VBS, constituting a rather passive form
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of risk assessment. After the USV died down, more active forms of risk assessment gradually appeared, including approach to the openings of the surface area. Rats might extend their heads closer and closer to these openings over time, orienting their eyes and ears to the surface, but without actually entering it (Blanchard and Blanchard, 1989). These observations fit well with an interpretation that circa 22 kHz USV in rats serve to warn colony members of the presence of danger, whereas risk assessment activities enable the subject to assess the likelihood of this danger, initially from a relatively safe location (the tunnel or burrow) and later, in the absence of any further indication of danger, with forays onto the surface itself. Thus, these behaviors, both emission of USV and risk assessment activities, serve as components of a defensive decision-making sequence, with USV promoting defensiveness and risk assessment reducing it (given that, as in these studies, the cat is no longer present). This process provides an indication of the essential conservatism of the defensive process in that the interval between the gradual phasing out of alarm USV in these colonies and the first entry of any rat onto the surface area was about five hours. Better safe than sorry. However, these behaviors did not end the defensive sequence. When the first rat (always the dominant) re-entered the surface area, it would quickly sprint across to the near corner of the open space, exiting one tunnel and entering another in a few seconds or less. Such “corner runs” may be an efficient way to assess the potential danger of a situation further, by soliciting an attack from the no-longer-visible threat source, when such attack is unlikely to be successful because the rat’s period of vulnerability is so short. As such, it may represent an additional form of risk assessment. Sex differences in emission of USV to a live cat included differences in the frequency and duration of emission, as well as in the sonographic characteristics of these calls, with females reliably producing more frequent and longer USV than males. While cat exposure produced high levels of USV in both sexes, perhaps indicative of a ceiling effect (maximal response), potential threats (cat odor alone) produced marked sex differences. Sonographic analyses showed consistent differences in the patterns of USV emitted by the two sexes. Females showed a mean frequency of 22.2 kHz with a narrow frequency distribution, while males showed a mean frequency of 20.1 kHz with a wider distribution, congruent
with the expected relationship between body size and vocalization frequency (see Fletcher, Chapter 3.1 in this volume). Six major subtypes of vocalizations were described based on the sonographic structure: horizontal; linear ascending; linear descending; U-shaped; negatively accelerated ascending; and negatively descending pulses. Females showed higher levels of horizontal, linear descending, U-shaped and negatively accelerated ascending USV, while males largely emitted negatively accelerated descending pulses. These sex differences are in accordance with the notion that in addition to their emotional content, 22 kHz USV carry significant informative value; it may be adaptive for females to produce more USV due to their care of pups, a particularly vulnerable group of conspecifics that may be closely related to the caller. Gender variation in the sonographic characteristics of alarm vocalizations may also provide a valid means of recognition of the caller’s gender or other features. The wide range of USV characteristics that show variation may also contribute to the identification of unique signals through which individual rats may be recognized. Recent studies of responses of rats to olfactory stimuli from cats indicated their ability to discriminate between individuals (Staples et al., 2008). These findings suggest that the complexity of 22 kHz vocalizations may provide a parallel in terms of individual identification of conspecifics.
II.B. Field studies Recent studies of animal communication question the classical distinction between the semantic communication of human language and the emotionrelated calls of animals. Field observations show that threat-linked animal vocalizations may be evaluated in terms of both their informative value, i.e., the reliability with which a call signifies the presence of a threat, and their referential specificity, i.e., the precision with which particular stimuli elicit a specific call type (Seyfarth and Cheney, 2003). The field literature contains many examples of vocalizations oriented toward conspecifics that include referential or descriptive information with reference to the source of threat and its characteristics. African meerkat sentinels (Suricata suricatta) (meerkat groups usually consist of 3 to 30 individuals) cease foraging and climb to high ground or to the tops of shrubs to assess better the danger of possible predator threats (Clutton-Brock et al., 1999). When such a
Vocalization as a social signal in defensive behavior threat is detected, meerkats emit alarm vocalizations that have been shown to convey information regarding both predator type and the urgency of danger to its group (Manser et al., 2002). Vocalizations of black-capped chickadees (Poecile atricapilla) convey predator size to conspecifics, subsequently modulating their defensive reactions (Templeton et al., 2005). Diana monkeys (Cercopithecus diana) produce differential alarm calls for aerial and terrestrial predators, as well as for predators, nonpredators and other general disturbances (Zuberbühler et al., 1997). Belding’s ground squirrels (Spermophilus beldingi) emit alarm calls that have been shown to be nepotistic warnings preferentially directed at relatives (Sherman, 1977); young squirrels learn to respond more quickly to calls signifying fast-moving predators than to those indicative of slow-moving ones, thus demonstrating both their referential value and their importance for survival (Mateo, 1996). Gunnison’s prairie dogs (Cynomys gunnisoni) produce four different types of alarm calls depending on the type of predator, which result in two different responses by conspecifics (Kiriazis and Slobodchikoff, 2006). Several species of marmots (Marmota flaviventris, M. olympus, M. caligata, M. monax) emit alarm calls directed towards pups in order to warn them of danger (Blumstein and Armitage, 1997, 1998; Daniel and Blumstein, 1998). The alarm calls of a number of species are modified by the immediacy of a threat, with distant threats eliciting one type of call and immediate threats a distinctly different call (Klump and Shalter, 1984; Macedonia and Evans, 1993). Similarly, defensive responses of Richardson’s ground squirrels (Spermophilus richardsonii) vary in accordance with the proximity of the conspecific caller, with neighbor squirrel calls eliciting higher levels of vigilance than non-neighbor calls, indirectly indicative of the threat urgency (Hare, 1998). A number of phenomena observed in rat VBS studies are supported by field work with other mammals. The dependence of vocalizations on the presence of conspecifics is in line with observations of similar calls in other rodent species (Blumstein and Armitage, 1997, 1998). Female Belding’s ground squirrels (Sherman, 1977) and marmots (Blumstein and Armitage, 1997, 1998) showed significantly higher alarm vocalizations, akin to findings showing enhanced levels of 22 kHz USV in female rats (Blanchard et al., 1992), observations suggesting greater adaptive value for female alarm calls as their young are more likely to be in close proximity. Meerkats and marmots emit alarm
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vocalizations from a place of relative safety. Similarly, rats in the VBS are more likely to emit USV from within the burrows. Field studies in meerkats (CluttonBrock et al., 1999) and marmots (Blumstein and Armitage, 1997) showed a link between dominance and risk assessment, suggesting that dominant animals are also more likely to produce alarm vocalizations. In the VBS, dominant males are more likely than subordinates to occupy the surface area, and as a result are more likely to first encounter threat-related stimuli, and to initiate alarm vocalizations.
III. Conclusions The study of defensive behaviors and their biology may be relevant to analysis of a number of human emotion-related behaviors. In this context, alarm vocalizations are particularly interesting as they may shed light on the social and communicatory aspects of anxiety and other threat-related emotions. Laboratory and field studies suggest that alarm vocalizations in a variety of species serve to convey both emotion and information related to the caller and the threat source. Their conservation over mammalian species, and in particular their strong association with species showing gregarious social systems, provide substantial support for a view that human alarm or warning vocalizations may provide a strong functional parallel to those of non-human mammals.
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