Stability of Acoustic Individuality in the Alarm Calls of Wild Yellow Ground Squirrels Spermophilus Fulvus and Contrasting Calls from Trapped and Free-Ranging Callers
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Naturwissenschaften (2010) 97:707–715 DOI 10.1007/s00114-010-0686-7 ORIGINAL PAPER Stability of acoustic individuality in the alarm calls of wild yellow ground squirrels Spermophilus fulvus and contrasting calls from trapped and free-ranging callers Vera A. Matrosova & Ilya A. Volodin & Elena V. Volodina & Nina A. Vasilieva Received: 16 April 2010 /Revised: 24 May 2010 /Accepted: 25 May 2010 /Published online: 18 June 2010 # Springer-Verlag 2010 Abstract The questions of individuality and stability of calls retain the cues to individuality between two encoun- cues to identity in vocal signals are of considerable ters of surrogate predators (humans), separated on average importance from theoretical and conservation perspectives. by 3 days. Discriminant function analysis showed that the While individuality in alarm calls has been reported for alarm calls of individual yellow ground squirrels were very many sciurids, it is not well-documented that the vocal similar within a recording session, providing very high identity encoded in the alarm calls is stable between individual distinctiveness. However, in six of the ten different encounters with predators. Previous studies of animals, the alarm calls were unstable between recording two obligate hibernating rodents, speckled ground squirrels sessions. Also, we examined ten dye-marked individuals Spermophilus suslicus, and yellow ground squirrels Sper- for consistency of acoustic characteristics of their alarm mophilus fulvus demonstrated that, after hibernation, most calls between the encounters of humans, differing in individuals could not be identified reliably by their alarm techniques of call collection, from free-ranging vs trapped calls. Moreover, in most speckled ground squirrels, indi- animals. We found differences only in two variables, both vidual patterns of alarm calls changed progressively over as related to sound degradation in the environment. Data are little as 2 weeks. However, these previous data have been discussed in relation to hypotheses explaining the adaptive obtained using the collection of alarm calls from trapped utility of acoustic individuality in alarm calls. animals. Here, we examined ten free-ranging dye-marked yellow ground squirrels to determine whether their alarm Keywords Spermophilus fulvus . Alarm call . Ground squirrel . Individual identity. Vocal stability. Electronic supplementary material The online version of this article Recording technique (doi:10.1007/s00114-010-0686-7) contains supplementary material, which is available to authorized users. V. A. Matrosova : I. A. Volodin Introduction Department of Vertebrate Zoology, Faculty of Biology, Lomonosov Moscow State University, Retention of individual vocal traits over time has been Vorobievy Gory, 12/1, studied across a variety of taxa for various reasons. Most Moscow 119991, Russia studies with nonpasserine birds have aimed to identify : I. A. Volodin (*) E. V. Volodina stable individual vocal signatures as fingerprints for Scientific Research Department, Moscow Zoo, monitoring rare or secretive species in nature (Lengagne B. Gruzinskaya, 1, 2001; Puglisi and Adamo 2004; Terry et al. 2005; Grava et Moscow 123242, Russia e-mail: [email protected] al. 2008; Klenova et al. 2009). For whales and dolphins, the main research focus was on stable vocalizations that serve N. A. Vasilieva individual recognition (Sayigh et al. 1990; Tyack 1997)or Severtsov Institute of Ecology and Evolution, as indicators of group identity (Ford 1991; Rendell and Russian Academy of Sciences, Leninsky pr., 33, Whitehead 2003). Studies with non-human primates have Moscow 119071, Russia concentrated on the effects of the social environment on the 708 Naturwissenschaften (2010) 97:707–715 sustainability of vocal structures (Jones et al. 1993; examining individuality in alarm calls (e.g., Koeppl et al. Snowdon and Elowson 1999; Rukstalis et al. 2003). For 1978; Hanson and Coss 2001; Blumstein and Munos 2005), ground-dwelling sciurids, the question of stability in vocal the documented temporal instability in the alarm calls of the signature over time (Matrosova et al. 2009, 2010) has been two ground squirrel species could be affected by a discussed mainly in relation to the abilities of conspecifics procedure of recording calls from trapped animals. Also, to discriminate individuals by their alarm calls based solely alarm calls produced by captive squirrels at least have the on the acoustic characteristics (Hare 1998; Blumstein and potential to be very different from free-ranging squirrels. Daniel 2004). These methodological points could not be addressed earlier Besides their primary function of warning conspecifics in that the retention of the vocal signature has yet to be of predators (Sherman 1977; Blumstein 2007) or warning studied in any free-ranging terrestrial mammal. Also, the predators that they have been detected by a caller alarm calls produced by trapped and free-ranging ground (Woodland et al. 1980; Sherman 1985; Hasson 1991; squirrels has not been compared. Digweed and Rendall 2009a,b), alarm calls of at least two Free-living yellow ground squirrels represent convenient species of marmots and five species of ground squirrels also subjects to study individuality encoded in alarm calls. provide concomitant information about the identity of the Yellow ground squirrels are the largest of the Spermophilus caller (Nikol’skii and Suchanova 1994; McCowan and species, with a body length without tail of 230–370 mm, a Hooper 2002; Blumstein and Munos 2005; Matrosova et al. body mass at emergence from the hibernation of 600– 2009, 2010; Schneiderová and Policht 2010). However, 900 g, and a body mass before hibernation of 1,600– selection pressures driving the evolution of individual 2,000 g. These squirrels live in patchy vegetation and thus distinctiveness in mammalian alarm calls are not yet clear can be observed visually (Ismagilov 1969; Efimov 2005; (Blumstein et al. 2004; Blumstein 2007). Two explanatory Matrosova et al. 2007; Vasilieva and Tchabovsky 2009). hypotheses have been advanced in this regard, the caller Information regarding the individual identity conveyed by reliability hypothesis and the multiple calling hypothesis. alarm calls is potentially important for this species, as According to the caller reliability hypothesis, the callers yellow ground squirrels demonstrate a male dominance producing false alarms in the absence of real danger should hierarchy during the mating period (Bokshtein et al. 1989), be considered as unreliable, and their alarms should be social play between litter mates, and prolonged affiliative ignored by conspecifics (Cheney and Seyfarth 1988; Hare contacts between mothers and offspring, up to hibernation and Atkins 2001; Blumstein et al. 2004). According to the (Vasilieva et al. 2009). multiple calling hypothesis, simultaneous alarms of multi- The alarm call of the yellow ground squirrel is the ple callers should result in higher responsiveness of loudest and most common call type and does not vary in conspecifics compared with those of a single caller, as they structure when produced in response to raptors, terrestrial signal enhanced urgency of response (Robinson 1981; predators, and humans (Nikol’skii 1979). It consists of Weary and Kramer 1995; Blumstein et al. 2004; Sloan frequency-modulated tonal notes, each of about 70 ms and Hare 2006, 2008). duration, with a maximum fundamental frequency of Both hypotheses share the common implicit assumption 5–6 kHz emitted in clusters of two to 16 notes (Fig. 1), that the alarm calls convey correct information concerning produced with inter-cluster intervals substantially longer the identity of a caller. The caller reliability hypothesis also than cluster duration (Nikol’skii 1979; Matrosova et al. rests on the assumption that individual vocal signatures 2007, 2010). Here, we examine individual distinctiveness should be stable at least for some time; otherwise conspecifics could not memorize and distinguish between reliable and unreliable callers. However, most individual speckled and yellow ground squirrels Spermophilus susli- cus and Spermophilus fulvus showed unstable alarm calls over a year (Matrosova et al. 2009, 2010) and among individual speckled ground squirrels calls proved unstable between predatory events separated by 2 days or by 2 weeks (Matrosova et al. 2009). Group inherent features, like age or sex, did not have significant effects on the retention of a stable alarm call structure in yellow ground squirrels (Matrosova et al. 2010). However, these findings were obtained with animals emitting alarm calls toward a human Fig. 1 Power spectrum (left) and spectrogram (right) of the alarm call cluster of the yellow ground squirrel (S. fulvus) consisting of four from live-traps. Although the collection of alarm calls from notes and measurements taken from the cluster and from the second animals sitting in live-traps is generally accepted for alarm call note (see text for description of parameters) Naturwissenschaften (2010) 97:707–715 709 and the short-term stability in the acoustic structure of the recordings from free-ranging and trapped animals was alarm call of free-ranging yellow ground squirrels. Also, we within the range of natural variation of propagation of examine individual characteristics in alarm calls, produced alarm calls throughout the colony to potential conspecific by the same individual yellow ground squirrels when or predatory receivers. On average, a recording session trapped and when freely ranging.