Whistle discrimination and categorization by the Atlantic bottlenose dolphin (Tursiops truncatus): A review of the signature whistle framework and a perceptual test

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Behavioural Processes 77 (2008) 243–268

Whistle discrimination and categorization by the Atlantic bottlenose dolphin (Tursiops truncatus): A review of the signature whistle framework and a perceptual test Heidi E. Harley a,b,∗ a

Division of Social Sciences, New College of Florida, 5800 Bay Shore Road, Sarasota, FL 34243, United States b The Seas, Epcot® , Walt Disney World® Resort, Lake Buena Vista, FL, United States Received 2 July 2007; received in revised form 6 November 2007; accepted 6 November 2007

Abstract Dolphin whistles vary by frequency contour, changes in frequency over time. Individual dolphins may broadcast their identities via uniquely contoured whistles, “signature whistles.” A recent debate concerning categorization of these whistles has highlighted the on-going need for perceptual studies of whistles by dolphins. This article reviews research on dolphin whistles as well as presenting a study in which a captive, female, adult bottlenose dolphin performed a conditional matching task in which whistles produced by six wild dolphins in Sarasota Bay were each paired with surrogate producers, specific objects/places. The dolphin subject also categorized unfamiliar exemplars produced by the whistlers represented by the original stimuli. The dolphin successfully discriminated among the group of whistles, associated them with surrogate producers, grouped new exemplars of the same dolphin’s whistle together when the contour was intact, and discriminated among same-contour whistles produced by the same dolphin. Whistle sequences that included partial contours were not categorized with the original whistlers. Categorization appeared to be based on contour rather than specific acoustic parameters or voice cues. These findings are consistent with the perceptual tenets associated with the signature whistle framework which suggests that dolphins use individualized whistle contours for identification of known conspecifics. © 2007 Elsevier B.V. All rights reserved. Keywords: Animal communication; Dolphin whistles; Whistle perception; Tursiops truncatus; Dolphin

Ron Weisman’s enthusiasm for studying auditory perception in songbirds and comparing it to other species conveys the joy, interest, and sense of discovery he clearly feels for his work. As he says about uncovering how birds discriminate among natural vocalizations, “I mean, now you really KNOW something!” Ron Weisman and his colleagues have enriched our knowledge of the perception of acoustic stimuli in many bird species (zebra finches, black-capped chickadees, mountain chickadees, Carolina chickadees, brown-headed cowbirds, white-throated sparrows) and highlighted the synergy created through the convergence of lab and field data focused on how animals negotiate their worlds (e.g., Bloomfield et al., 2003; Friedrich et al., 2007; Hurly et al., 1992; Johnsrude et al., 1994; Lee et al., 2006; Lohr et al., 1994; Sturdy and Weisman, 2006; Weisman et al., 1998,

∗ Correspondence address: Division of Social Sciences, New College of Florida, 5800 Bay Shore Road, Sarasota, FL 34243, United States. Tel.: +1 941 487 4328; fax: +1 941 487 4475. E-mail address: [email protected].

0376-6357/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2007.11.002

2004). A similar synergy has emerged from work on dolphin whistles. Lab and field studies have intersected in their findings on dolphins’ individualized and shared whistles (Caldwell and Caldwell, 1965; Caldwell et al., 1990; Cook et al., 2004; Gish, 1979; McCowan and Reiss, 1995b, 2001; Sayigh et al., 1990, 1995), auditory perception and categorization (Caldwell et al., 1969, 1971b; Herman, 1975; Herman and Arbeit, 1972, 1973; Herman and Gordon, 1974; Herman and Thompson, 1982; Herman et al., 1984; Ralston and Herman, 1995; Sayigh et al., 1998; Thompson and Herman, 1975, 1977, 1981), vocal learning abilities (Caldwell and Caldwell, 1972; Fripp et al., 2005; Hooper et al., 2006; Janik, 2000a; Lilly, 1965; Miksis et al., 2002; Reiss and McCowan, 1993; Richards et al., 1984; Sigurdson, 1993; Smolker and Pepper, 1999; Tyack, 1986; Watwood et al., 2004), and whistle function (Janik and Slater, 1998; Janik et al., 2006; Smolker et al., 1993; Watwood et al., 2005). This article reviews the literature on Atlantic bottlenose dolphin whistles to highlight for the reader how questions from observational studies compel laboratory studies on perception of natural vocalizations. [Although many dolphin species whis-

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tle, and some species appear to have whistles that may function similarly to those of the bottlenose dolphin (e.g., Caldwell et al., 1973), only data concerning the Atlantic bottlenose dolphin will be reviewed here because this species has been studied most comprehensively. In this paper the term “dolphin” refers to the Atlantic bottlenose dolphin, Tursiops truncatus.] The review concludes with a study of dolphin perception of conspecifics’ whistles. Sound energy is transmitted very efficiently in water, and dolphins have developed remarkable acoustic production and reception systems. They hear across a very wide frequency range, from 75 Hz to 150 kHz (Johnson, 1968), with individual variation (Ridgway and Carder, 1997). They have a unique production system that includes a system of air sacs that can recycle air (Cranford et al., 1996) and may be affected by depth; in one controlled study, two beluga whales’ whistles were softer and higher frequency at 200 m depth than at 5 m depth (Ridgway et al., 2001). Dolphins produce a variety of vocalizations typically divided into narrowband whistles and broadband echolocation clicks and burst pulses. Echolocation clicks appear to be primarily used for investigating the environment (see Au, 1993, for a review), although they may have social uses too (e.g., Xitco and Roitblat, 1996). Burst pulses are not well studied, but their primary function may be social (Blomqvist and Amundin, 2004; Gish, 1979; Lammers et al., 2003; Overstrom, 1983). Other sounds that may or may not fit into the above-mentioned categories have been idiosyncratically described through the years as squawks, mewings, blats, and more. (See Ralston and Herman, 1989, for a concise and erudite review of dolphin vocalizations and auditory perception.) Recently, Dos Santos et al. (1995) described low-frequency “bray” calls that Janik (2000b) found to

be correlated with dolphins feeding on salmonids; McCowan and Reiss (1995a) described a wide-band, low-frequency vocalization, “thunk”, produced by captive dolphin mothers when their infants moved away from them; Connor and Smolker (1996) described a series (6–12 s−1 ) of low-frequency “pops” apparently used by males when a herded female strayed. However, the most studied dolphin social vocalizations are the narrowband whistles. Whistles stand out in dolphin vocal emissions because they are narrowband, relatively low frequency, and fairly loud (Ralston and Herman, 1989; Tyack, 1986). Whistles from 3.5 to 10 kHz can be perceived by dolphins that are up to 25 km away from the whistler when seas are shallow and calm (Janik, 2000c). These attributes appear to make whistles ideal as contact calls in this marine species (Ralston and Herman, 1989; Tyack, 2000) that participates in a fission–fusion society apparently built upon the maintenance of long-term social ties in a complex environment (Wells, 1991, 2003). However, because the dolphin’s production system is still somewhat mysterious, we do not know if “voice” cues, typically available to terrestrial mammals, exist for dolphins (Ralston and Herman, 1989; Tyack, 2000); in fact, one study shows that voice cues are not necessary for dolphin discrimination of conspecifics’ whistles (Janik et al., 2006). A major issue for researchers of dolphin whistles concerns the mechanisms that dolphins may use for individual recognition. Some of the earliest work on dolphin whistles suggested an unusual mechanism for individual recognition. In one of the first studies of dolphin whistles, Dreher (1961) recorded a group of dolphins and drew attention to dolphins’ whistle contours, changes in frequency over time (Dreher, 1961). Later Caldwell

Fig. 1. Spectrograms illustrating the frequency contours of the original whistle stimuli. Frequency is on the vertical axis and time is on the horizontal access.

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and Caldwell (1965) recorded isolated dolphins in order to identify the whistlers, and they were struck by an unexpected finding: Each dolphin appeared to produce a preponderance of whistles with one contour that was unique to that dolphin. (See Fig. 1 for examples of whistle contours.) These whistles came to be known as “signature whistles”, and this finding had a strong influence on all later work concerning dolphin whistles. An umbrella article summarized a great deal of the Caldwells’ work (Caldwell et al., 1990). Their large corpus of 22,278 whistles was recorded from 126 captive dolphins (7 born in captivity) of all ages and sexes and revealed that, in general, each dolphin tended to produce a predominant whistle contour, the signature whistle. Animals were usually, but not always, isolated. When in a group, whistlers were identified when they were near the surface or, “as a last resort”, when there was a whistle and a concurrent bubble stream emitted through the blowhole. The authors categorized partial segments of signature whistles into the signature whistle category, and repetitive loops (an iteration of the same or similar contour that may have differentiated introductory and terminal loops) separated by very short pauses of stable duration as a single utterance. When possible, more than one observer, using spectrograms, scored the whistles for contour similarity. Using this categorization scheme, 117 out of 120 dolphins each produced an individualized contour more than half the time; 102 dolphins produced their signature whistles in 90% or more of their whistle productions. The range was from 0 to 100%, and the average was 94%. Newborns did not each produce mostly one unique contour, but most did so by the end of their first year of life. When individualized predominant contours were produced in the first year, they generally consisted of a single loop. (See Fig. 1, Dyad1, for an example of a single-loop whistle.) Adult dolphins typically produced more than one loop; multi-loop whistles (example in Fig. 1, Daughter) could include fractional loops (e.g., 1.5 whistles). Whistle frequencies ranged from 1 to over 24 kHz; the mode was 7 kHz. Frequency modulation increased with the age of the dolphin. Adult males whistled least often. Average whistle duration was 0.96 s. Signature whistles of three dolphins recorded across years suggested stability in contour over long (>17 years) periods. Although an individual’s predominant contour remained stable, some parameters changed across utterances including changes in rate, intensity, duration, and sudden terminations. The authors hypothesized that the whistle could broadcast the identity and location of a dolphin to its social group and that variations of parameters could convey other information about the whistler, but variations among an individual’s contours were idiosyncratic. To interpret them would require knowledge of an individual’s typical whistle. Most current work on dolphin whistles is still based on the Caldwells’ original suppositions, although the framework within which signature whistles have been evaluated has evolved over time. The over-arching premise is that dolphins are members of large social communities and need a way to identify each other across expanses of murky water. Due to their unusual adaptations for sound production in water and/or loss of signal fidelity across distances, they may not broadcast voice cues when they vocalize. To compensate, dolphins use their sophisticated vocal apparatus to produce individualized whistle contours that are

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products of each dolphin’s social and acoustic environment. To respond to social pressures and changing relationships with conspecifics, contour production needs to be flexible. Variations across emissions of a single dolphin’s individualized identifying whistle contour may convey useful state information that may lead to differential responses (e.g., immediate congregation or maintenance of on-going behavior) from listening conspecifics. This theory of individual recognition by whistle contour implies that (1) each dolphin has a unique whistle contour, the signature whistle, that it whistles frequently when the dolphin is separated from its social group, (2) dolphins use signature whistles in contexts in which they need to broadcast identity/state information, and, at least in the main, other whistles do not broadcast identity information, (3) dolphins learn their signature whistles, (4) dolphins can discriminate among a group of dolphins’ signature whistles, (5) dolphins can both group samecontour whistles together and discriminate among same-contour whistles produced by one dolphin, and (6) dolphins can associate signature whistles with specific whistlers. Some of these statements have garnered more supporting evidence than others. Numerous researchers have corroborated and expanded many of the Caldwells’ findings related to these issues, although the majority of later studies have reported a larger whistle repertoire for individuals. In most of these studies a “signature whistle” is defined as the whistle contour most commonly produced by an isolated individual dolphin. Recent work by one team of researchers (McCowan and Reiss, 1995b, 2001) has called into question the usefulness of the signature whistle framework. Specifically, McCowan and Reiss suggest that all dolphins may use a single contour, the upsweep/rise (low frequency to high), as the primary whistle contour for individual identification rather than an individualized contour, the signature whistle. One goal of the following review is to determine whether these apparently contradictory perspectives on dolphin whistles can be integrated. The review addresses the major issues covered within the signature whistle framework: whistle contour/repertoire acquisition, contextual use of whistles, whistle perception, and whistle production. Reporting of upsweep/rises and individualized signature whistles are considered throughout the review. Given the current debate on the existence of signature whistles, studies are presented in some detail to allow the reader to get a sense of the numbers of dolphins, contexts, and methods used. In this review I often use the term “predominant” whistle to indicate a dolphin’s most frequently produced whistle contour as judged by the author of the study under discussion. At the end of the review, I present a study of whistle perception conducted with a bottlenose dolphin subject. 1. Whistle contour/repertoire acquisition Data on whistle ontogeny, whistle repertoire, and whistle matching suggest that whistle contours are learned (Caldwell and Caldwell, 1979; Caldwell et al., 1990; Gish, 1979; Graycar, 1976; Fripp et al., 2005; Janik, 2000a; Miksis et al., 2002; McCowan and Reiss, 1995b,c; Sayigh et al., 1990, 1995; Smolker and Pepper, 1999; Tyack, 1986, 1993; Watwood et al., 2004).

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1.1. Whistle ontogeny Young dolphins produce a variety of whistle contours many of which are unique to a specific dolphin. An analysis of whistles produced by eight captive bottlenose dolphins freely swimming during their first year of life led to the identification of 128 contour-based whistle types determined using analyses based on contours represented via 20 frequency points measured at equal intervals as pioneered by McCowan (1995) (McCowan and Reiss, 1995c). Whistles were attributed to individual whistlers based on concurrent whistling and visible bubble streams. Of the identified whistles, 23% of the contours were produced by two or more dolphins, and 73% were unique to individuals. Eleven whistle types were produced by infants and adults in three different social groups; one of these types was the upsweep/rise reported in many papers on dolphin whistles (Dreher, 1966; Lang and Smith, 1965; Janik et al., 1994; McCowan and Reiss, 1995b; Smolker and Pepper, 1999; Tyack, 1986; Watwood et al., 2004, 2005). Two whistle types, including the upsweep/rise, accounted for 66% of the infants’ whistles. Across the first year of life, the infant repertoire changed dramatically with a turnover rate from 70 to 86%. The development of calves’ predominant whistles appears to be influenced by whistles in their community. Five wild dolphin calves observed during their first four months of life and recorded a year or more later developed predominant whistle contours that were most similar to predominant whistles produced by dolphins within their communities with whom they had had little contact (Fripp et al., 2005). Calves’ predominant whistles were compared to predominant whistles produced by dolphins within and beyond the calves’ community using a dynamic time-warping procedure that fit one contour to another and produced a similarity score for each pair-wise comparison (Buck and Tyack, 1993); of the 32 similar contours, 30 were from the calves’ community members. Each calf’s whistle was similar to about six other predominant whistles. Ninety percent of the dolphins with similar whistles were seen within 50 m of the calves less than 5% of the time that calves were observed. Trainers’ bridges, whistles used as secondary reinforcers, may influence the development of captive dolphins’ predominant whistles. The most commonly occurring predominant whistle contours from each of 10 dolphins born and raised at the Miami Seaquarium were compared to predominant whistle contours produced by wild Sarasota Bay dolphins matched for age and sex (Miksis et al., 2002). Dolphin whistles were also compared to trainers’ bridges which typically have a flat contour. Comparisons using a variety of techniques (spectrographic measurements; the dynamic time-warping technique designed by Buck and Tyack, 1993; mathematical estimates of modulation rates) revealed that trainers’ whistles had the flattest contours, and captive dolphins’ whistles were significantly flatter than those of wild dolphins. Wild dolphins’ whistles were more highly modulated than captives’ whistles. Trainers’ whistles occurred at a much lower rate than most dolphins’ whistles, although trainers’ whistles were paired with food and may have been particularly salient.

Male calves may be more likely to produce whistles similar to their mothers’ whistles than female calves (Sayigh et al., 1995). Human raters used spectrograms to make pair-wise similarity judgments of whistles produced by 21 male calves and their mothers as well as 21 female calves and their mothers. Ratings ranged from 1 (not similar) to 5 (very similar). The 15 female calves produced whistles that were rated as being not similar to their mothers’ whistles whereas only 7 of the male calves’ whistles were rated as being not similar to their mothers’ whistles. In the same vein, 2 of the 21 female calves’ whistles were considered very similar to their mothers’, whereas 9 of the 21 male calves’ whistles were considered very similar to their mothers’ whistles. Overall similarity ratings were significantly higher for whistles of mothers and male calves versus female calves. Adult females in Sarasota Bay are more likely to associate with their mothers than are adult males. Adult males tend to associate with females for very short periods of time unless the females are receptive (Wells, 2003). In contrast, adult females are likely to associate with other females in the same reproductive state, i.e., pregnant, receptive, resting, raising calves of similar age (Wells, 2003). Because dolphins are long-lived and females tend to stay in the same geographical area, adult mothers and daughters are more likely to spend extended periods of time together than are adult mothers and sons. Easily discriminable whistles in mothers and daughters may lead to fewer confusions, and similar whistles in mothers and sons may facilitate kin recognition and the avoidance of inbreeding (Sayigh et al., 1990, 1995). Adults’ predominant whistle contours tend to be more complex than those of young dolphins. In a study of predominant whistles produced by 14 dolphins in their first year of life, these young dolphins were much more likely to produce single-loop whistles than were adults; adults typically produced multilooped predominant whistles (Caldwell and Caldwell, 1979). Adult dolphins in the wild are likely to produce more elaborate predominant whistles than are calves (Sayigh et al., 1990). Adult dolphins’ predominant whistle contours generally remain stable across years. Both in captivity (Caldwell et al., 1990) and in the wild (Sayigh et al., 1990; Watwood et al., 2005) predominant contours have been the same for individuals for up to 16 years. However, whistle contours may be influenced by a dolphin’s regular associates, and so when those associates change, preferred contours may change slightly (Watwood et al., 2005). Although individual dolphins’ predominant whistles can be similar to each other, a variety of categorization schemes (discussed in Section 3.1 below) suggests that they are typically discriminable from those of another dolphin. In one study a comparison of human similarity judgments of predominant whistles highlighted that the predominant whistles of individuals were always more similar to each other than to those of other dolphins (Watwood et al., 2004). 1.2. Whistle repertoires Contours of predominant whistles are more similar between male partners than between non-partnered males (Watwood et al., 2004). Adult male dolphins form long-term pair bonds

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(Smolker and Pepper, 1999; Wells, 1991, 2003). In these dyads, rates of association between members are very high; they are usually seen together (Owen et al., 2002). In Watwood et al.’s (2004) study 15 male dolphins representing 9 dyads (some individuals participated in more than one dyad due to partner deaths) were recorded in a temporary capture/release program that was part of a long-term study of dolphin behavior and health conducted by Wells and his associates in Sarasota Bay, FL (Wells, 1991, 2003). Two adult females were also recorded as a control. Every dolphin produced one contour more often than others ranging from 47 to 100%. The dolphins produced 125 whistle types of which 88 (70.4%) were unique to individuals; 10 contours were shared only by a single pair of dyad members and 27 were shared more broadly. Dyad members shared 45% of their whistle loop types with their partners, but each dolphin only shared 25% of its whistle loop types with the other individuals in the study. In pair-wise quantitative and qualitative comparisons of whistle pairs between and across 10 dyad members, 7 of 10 males had preferred contours that were rated as being more similar to partners’ whistles than to non-partners’ whistles. Another study focusing on male associates tracked the whistle repertoires of three wild male dolphins that were recorded in an area where they were provided with fish by humans at a beach in Australia (Smolker and Pepper, 1999). The individuals’ whistle repertoires became significantly less variable over four years of increasing association. Eighteen major whistle contours were counted across the four years. In 1987 and 1988 roughly the same number of whistles was recorded for each dolphin. In 1987, 19 (2.7%) of the whistle contours produced were of two whistle types. In 1988, the final year of the study, 252 (35.29%) of the whistle contours produced were these two contours. Whistles may also reflect regional differences. Graycar (1976) evaluated predominant whistles recorded from 158 captive Atlantic bottlenose dolphins captured from six different geographic regions off Florida’s coast. A discriminant analysis of the whistles suggested that sex–age groupings for some dolphin groups could be predicted based on whistle characteristics. In addition, 46% of the whistles were correctly classified based on the native region of the whistler; because there were six regions, chance performance was 17%. These data indicate that there are dialect differences in whistles produced by dolphins in different locales. Graycar tried to train a dolphin to differentiate between whistles from different regions (the Gulf off northwestern Florida and the Atlantic off northeastern Florida), but the dolphin was unsuccessful after 2300 trials. In Graycar’s (1976) study, no single parameter was central to his whistle classification via discriminant analysis; rather a combination of parameters was necessary. Whistle repertoire is also affected by whistle matching, i.e., one dolphin whistling a companion’s predominant whistle contour. 1.3. Whistle matching Dolphins who commonly associate will whistle each other’s predominant whistle contours. An adult male dolphin, Scotty, and an adult female dolphin, Spray, wore light-emitting diodes

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on their heads that lit up differentially based on the intensity of received sound waves (Tyack, 1986). Human observers reported when the “vocalights” were lit and recorded the dolphins’ whistles; whistles, represented spectrographically, produced both when the dolphins were and were not wearing vocalights were analyzed. (In a brief analysis of the Bubble-stream method of whistle attribution, Tyack noted that the dolphins produced bubble streams from their blowholes concurrently with whistles in only 11% of the cases; if Tyack had only used bubble streams to identify whistlers, most whistles would have been ignored.) Each dolphin produced its own predominant contour most often; segments of these contours were occasionally produced alone. There were also several other contours that occurred often enough to be cataloged: an upsweep/rise, a flat whistle, a downsweep, and a sine wave. Other variant whistles were lumped together. The majority of Spray’s whistles, 67%, were her predominant contour, 19% were Scotty’s predominant contour, and 14% were the other contours combined. Forty-eight percent of Scotty’s whistles were his predominant contour, 21% were Spray’s predominant contour, and 31% were the other named contours combined. Twice Scotty produced the flat contour immediately after the trainer produced his flat bridge, although Scotty’s productions were a higher frequency than the trainer’s. When Spray produced Scotty’s most common whistle contour, Spray’s productions tended to have a different amplitude modulation than did Scotty’s. Because original repertoires of each dolphin before cohabitation were not known, we cannot tell if both of these predominant contours were part of Scotty’s and Spray’s original repertoires (Tyack, 1986). If the contours were not part of the original repertoires, then the dolphins likely learned each other’s predominant whistles through imitation; dolphins can vocally imitate (Richards et al., 1984). If the contours were in the original repertoires, then whistle matching may have occurred through some other mechanism, e.g., social contagion or learning of contextual use. One dolphin may produce another dolphin’s predominant whistle in order to establish antiphonal (responsive) calling with that dolphin. Tyack (1993) recorded the vocalizations of a temporarily restrained wild 34-year-old female dolphin, Niklo, who was physically but not acoustically isolated from a group of five conspecifics. During the first half-hour of her hour-long restraint, Niklo produced over 500 of her own predominant whistles and no apparent reproductions of the predominant whistles associated with the other five dolphins including the oldest dolphin, Granny. However, during the second half hour, Niklo produced 47 instances of Granny’s predominant whistle contour. An analysis of the whistles of the other five dolphins revealed that whistles of Granny’s contour were produced from those dolphins (the group was recorded altogether; individual emissions could not be determined) in association with Niklo’s production of the same contour. In a study of whistle matching in unrestrained wild dolphins, dolphins monitored via non-invasive shore observations and a hydrophone array produced 39 matching whistle interactions in which whistles with the same frequency contour (as determined by human judges sorting spectrographic contour extractions) issued from multiple dolphins within 3 s of each other (Janik,

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2000a). Matching interactions occurred when dolphins were separated by a maximum of 579 m. Measurement limitations did not allow the identification of matching interactions when dolphins were closer than 26 m, therefore, it is likely that more matching interactions occurred. If dolphins use whistle contour to identify individuals, then the question of how dolphins recognize a whistler producing another dolphin’s predominant contour arises (Janik, 2000a). The answer may lie in context; if one dolphin typically reproduces another’s contour in an exchange between those two dolphins then identity could be easy to track. The study of the contextual use of whistles has been productive. 2. Contextual use of whistles Whistling and whistle exchanges occur most often when dolphins are separated and include a high proportion of individually predominant whistle contours compared to periods when dolphins are in groups, thereby suggesting that individually predominant whistles are used for identification and cohesion (Cook et al., 2004; Gish, 1979; Janik et al., 1994; Janik and Slater, 1998; Lang and Smith, 1965; McCowan and Reiss, 1995b, 2001; Sayigh et al., 1990; Smolker et al., 1993). Whistles often occur in a series of exchanges between separated dolphins. In one study, a five-year-old male dolphin, Dash, and a five-year-old female dolphin, Doris, were connected via an acoustic link that could be turned on or off (Lang and Smith, 1965). When the link was open, the dolphins whistled much more often (394 utterances) than when it was closed (68 utterances). Whistles were analyzed using waveforms, spectrograms, and by ear. The dolphins shared four whistle contours, and each had a unique whistle contour. The individually specific contours were most likely to be used in a whistle exchange, and, in later playbacks of Doris’s vocalizations to Dash, Dash tended to emit his individual contour in responses to Doris’s. Wild dolphins who are separated also engage in whistle exchanges. Temporarily restrained Sarasota Bay mothers and calves that were physically separated but acoustically available usually whistled their predominant whistles antiphonally during these separations (Sayigh et al., 1990). Antiphonal vocalizations appear to be category specific. In another study of separated captive dolphins in which tanks were acoustically linked, exchanges over the link were antiphonal, and overlapping almost never occurred (Gish, 1979). The dolphins produced both burst pulses and whistles, but exchanges were almost always of a single category, i.e., either whistles or burst-pulse exchanges occurred. In addition, context had a significant effect; dolphins who were together whistled much less often than separated dolphins. A group of six dolphins vocalized very little when they were together without an acoustic link to tanks with other dolphins (0.06 vocalizations/min) versus when they had an acoustic link to tanks with other dolphins (45.3 vocalizations/min). Whistles were also clearly social; dolphins isolated in tanks that had an acoustic link to tanks with other dolphins vocalized substantially less when the link was turned off (0.001 vocalizations/min) than when the link was turned on (50.4 vocalizations/min). A discriminant analysis

resulted in categorization of whistle contours by the dolphin that produced them providing support for the existence of individualized whistles. Some whistle matching between tanks also took place. Mother–infant reunions in Australia’s Shark Bay appeared to be mediated by predominant individualized-contour whistles (Smolker et al., 1993). Six mother–calf pairs were followed and recorded. Calves ranged in age from 0.5 to 3.5 years. Some calves produced predominant whistles that could have been categorized as upsweep/rises. For 2 mother–calf pairs, only about 7–8% of whistling occurred when a pair was together and 57–76% of whistling occurred during far (>20 m apart) separations. Although no multi-hydrophone acoustic localization techniques were used to identify whistlers, whistles during mother–calf separations were analyzed. During these separations most whistling appeared to be initiated by the calves that tended to begin whistling about halfway into the separation and usually stopped just before beginning to reunite with their mothers. Mothers appeared to whistle little in normal separations, although in two instances when mothers and calves were separated by male herding of the mothers, the mothers produced their predominant whistle contours very frequently. Undisturbed free-ranging dolphins in murky Sarasota Bay whistled differentially by context (Cook et al., 2004). Of 3208 whistles recorded via a hydrophone array dragged behind a boat, 52% were likely individually predominant whistles, 19% were upsweep/rises and 29% were other whistles. Whistles occurred more often when dolphins were socializing and typically spread out over a broader area than when they were traveling, an activity when animals are usually closer to each other. Isolation affects the distribution of whistle types produced. One isolated captive seven-year-old female dolphin produced 1743 whistles in three contexts: when she was alone and not being trained, after she had made a correct choice in a visual successive reversal task, and after she had made an incorrect choice in the task (Janik et al., 1994). Her whistling rate increased significantly after the incorrect choice (from about 8 whistles/min in other contexts to 12.7 whistles/min after an error). In all contexts, one contour was most frequent; however, 80% of her whistles outside of training were these predominant-contour whistles whereas only a little over half the whistles were predominantcontour whistles in the other contexts. The second most common contour was the upsweep/rise which comprised 9% of the whistles in the non-training context and a little over 20% of the whistles in the other two contexts. The predominant whistles varied by context. When the dolphin was not being trained, the whistles began at a lower frequency (1.1–1.5 kHz lower), ended at a high frequency (1–1.0 kHz higher) and were slightly shorter; the duration shift occurred in the last half of the whistle thereby changing the frequency contour slightly. The upsweep/rise contour also varied across conditions; it began at a slightly lower frequency in the non-training context. Another study compared predominant whistle-contour use within a group and between separated group members. Whistles from four captive dolphins (an adult male, an adult female, a 7-year-old male, and a 3.5-year-old female) were recorded when they swam together and when a single individual chose

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to leave the group to swim in another tank (Janik and Slater, 1998). Overall whistle rates did not vary by condition, but rates of specific contours did. The most common whistle for a separated individual was its predominant whistle: 68% for the adult male, 32% for the adult female, 92% for the sub-adult male, 73% for the juvenile female. When all animals were together, 2.4% of their whistles were predominant whistles. When three animals were together and another was separated, 56% of the remaining group’s whistles were predominant whistles. During separations predominant whistle matching only occurred five times; matching could not be identified for individuals in a group. Similar results occurred with wild dolphins (Watwood et al., 2005). Six Sarasota Bay dyads were recorded via suction-cup hydrophone when they were temporarily restrained and via a boat with a hydrophone array when they were free-swimming. Free-swimming whistlers were identified using photo identification and algorithms for sound localization. When male dyad members were together, they whistled infrequently. When they were separated via temporary capture, these males each produced a predominant and unique whistle contour. When they were free-swimming, about half of the whistles produced by 11 of 13 animals had also been produced when temporarily captured. Of these whistle productions occurring in both contexts, 76% were individuals’ predominant whistle contours. Individually predominant contours, stable for up to 16 years, were most likely to occur when these free-swimming animals were separated. Some predominant contours were upsweep/rises, but most were not. Two dolphins produced the upsweep/rise at low rates. Recent analyses of randomly sampled whistles from isolated wild dolphins verify the production of individually predominant contours in this isolation context (Sayigh et al., 2007). From a library of recordings of over 150 wild dolphins in Sarasota Bay, whistles from 20 randomly chosen dolphins were analyzed. The recordings were collected using suction-cup hydrophones attached to dolphins during temporary capture in Wells and his colleagues’ study of these dolphins since 1970 (Wells, 1991, 2003). Twenty whistles were randomly chosen from between 200 and 2144 whistles recorded in 1–2 recording sessions with each dolphin. Whistles separated by less than 0.25 s were treated as a single multi-loop whistle. Ten human subjects without experience viewing spectrograms were told to sort standardized-axes spectrograms into as many groups as desired using contour shape (and not number of iterated loops) as the major parameter; sorters did not know how many dolphins had produced the whistles. Overall, the sorters grouped 18.9/20 whistles for each dolphin by whistler; these groups included an average of 0.45 whistles produced by another dolphin. Given that these whistles were randomly selected from isolated whistlers (dolphins temporarily captured) and sorted by whistler with no information as to the number of dolphins recorded, these findings are a powerful demonstration that each dolphin produces a uniquely contoured whistle in this context. Yet again, dolphins recorded in free-swimming social groups apparently produced a low proportion of individualized whistle contours (McCowan and Reiss, 1995b). However, the upsweep/rise whistle found in other studies (Cook et al., 2004; Dreher, 1966; Janik and Slater, 1998; Janik et al., 1994; Lang

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and Smith, 1965; Smolker and Pepper, 1999; Tyack, 1986; Watwood et al., 2004, 2005) occurred frequently. Whistles from 10 undisturbed captive adult dolphins from three different social groups (tanks or facilities) were identified with the whistler based on whistles concurrent with bubble streams produced by the whistler’s blowhole (McCowan and Reiss, 1995b). Roughly 20 whistles from each dolphin were analyzed in multiple ways including McCowan’s (1995) quantitative contour analysis method. This analysis led to the identification of 29 whistles types. Of 185 whistles, 97 (52.4%) were upsweep/rises. For 7 of the 10 dolphins, the upsweep/rise was the most commonly produced contour. Two dolphins produced a different contour at an equal percentage with the upsweep/rise, and one dolphin produced another contour most often. Two or more dolphins within or across social groups shared 10 whistle contours, and the remaining 18 contours were unique to an individual. McCowan and Reiss (1995b) concluded that “signature whistles may play a less predominant role than previously suspected” (p. 207) perhaps in part due to the socially interactive context. That McCowan and Reiss (1995b) only analyzed whistles that occurred with concurrent bubble streams may have affected their results. Recently, an analysis of whistles produced with and without concurrent bubble streams by three adult captive female dolphins and their three newborn calves suggested that “bubble-stream whistles” were context dependent (Fripp, 2005). Bubble-stream whistles were rare; out of 19,488 whistles, only 217 (1%) were associated with bubble streams. Calves were much more likely to produce bubble streams with their whistles; 0.9% of calves’ whistles occurred with bubble streams compared to only 0.2% of adults’ whistles. Bubble-stream whistles also tended to occur in bouts: 49% within 1 s of another by the same whistler and 70% within 5 s of another by the same whistler. Of these, 72–75% had similar frequency contours and could not be considered independent of each other (Fripp, 2005). Multiple cluster analyses of whistles produced with and without bubble streams showed that bubble-stream whistles clustered together and many clusters did not include any bubble-stream whistles; some frequency contours never occurred with bubble streams. Not only did calves produce more bubble-stream whistles than did adults, but adults were much more likely to produce bubble-stream whistles when caring for a calf: In only 34% of the samples the adults were caring for their calves; however, 81% of their bubble-stream whistles occurred during those samples. Hence, an analysis of bubble-stream-only whistles would result in context-dependent whistles with fewer types of frequency contours and a heavier percentage of same-contour whistles. In a later study, McCowan and Reiss (2001) relied less heavily on bubble-stream whistles. They recorded whistles from 12 dolphins (including 4 dolphins from McCowan and Reiss, 1995b, and from McCowan et al., 1998) from three captive social groups in a variety of settings: voluntary isolation in the same pool, voluntary isolation in a separate pool, and temporary-capture poolside. The temporary-capture whistles were not accompanied with bubble streams, but these whistles were deemed similar to the other whistles and all whistles were lumped together for analysis; no specific information about the bubble-stream/nonbubble-stream whistle analysis or whistle context was provided.

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Whistles were sorted by people who were na¨ıve to the identity of whistler and context as well as by McCowan’s contour analysis method updated to use 60 (versus the previous 20) frequency measurements distributed across the whistle contours. Upsweep/rises were categorized into subcategories in a similar manner. Ten of twelve dolphins produced the upsweep/rise contour more often than any other contour. (One dolphin only produced one whistle during the recordings—an upsweep/rise.) A discriminant analysis of upsweep/rise contours produced by five individuals classified whistles by producer with fair accuracy (from 40 to 100%). Of the two dolphins with other predominant contours, one produced that contour for 71/115 (61.7%) whistles, and the second produced that contour for 9/9 (100%) whistles. In this study human observers and the revised 60-point contour analysis method categorized contours comparably. Somewhat surprisingly, McCowan and Reiss (2001) concluded, “Thus, individual variability in the production of a shared contact call, as reported for other taxa, probably accounts for individual recognition in dolphins” (p. 1151). McCowan and Reiss (2001) argued that none of these dolphins produced signature whistles in isolation. However, the definition of a signature whistle is the whistle contour produced most often by a dolphin in isolation (Janik and Slater, 1998; Smolker et al., 1993; Watwood et al., 2004, 2005). All of McCowan and Reiss’s (1995b, 2001) dolphins emitted a predominant whistle contour. Across the two studies, 18 dolphins were recorded and some produced few whistles. For example, in the second study, 1 dolphin produced 1 whistle (1/1, 100%, an upsweep/rise), and 1 produced 5 whistles (3/5, 60%, an upsweep/rise). Of these 18 dolphins, 13/18 (72.22%) produced the upsweep/rise most often and 5/18 (27.78%) produced another whistle contour equally or more often. McCowan and Reiss (2001) found that the upsweep/rises could be categorized by whistler fairly well. As opposed to concluding that individual recognition in dolphins was based on one shared contour, one could have concluded that some of these dolphins produced upsweep/rises as signature whistles. This phenomenon appears to occur in other dolphins. For example, in the study of whistles produced by adult male dyads living in Sarasota Bay described earlier (Watwood et al., 2004), occurrences of the upsweep/rise were addressed specifically in all analyses. Upsweep/rises were represented in 5 of the 125 contours and produced 32.65% of the time. Nine of the 17 dolphins (52.9%) recorded produced an upsweep/rise most often. Quantitative techniques (McCowan, 1995; McCowan and Reiss, 2001; Smolker and Pepper, 1999) and human pattern recognition skills were employed to determine similarity between predominant whistles based on three exemplars each from 10 dolphins; similarity measures from both techniques were highly correlated. Human judges used a 5-point scale from least similar (1) to most similar (5). Whistles from 4 of the dolphins rated were upsweep/rises. Upsweep/rises produced by a single dolphin were always more similar to each other (from 4.22 to 4.74 out of 5) than to upsweep/rises produced by other dolphins (from 2.67 to 4.04). Similarly, in another study in which five predominant whistles were compared (Buck and Tyack, 1993), two or three appear to be upsweep/rises. All of these

were successfully categorized by whistler. What may appear to be unique in one categorization scheme may be lumped together in another. Categorization of whistles is a formidable issue for researchers studying dolphin whistles. 3. Signature whistles? In all of the studies previously described researchers have had to categorize the dolphins’ whistles. Such categorization requires multiple decisions by researchers for every method available; human judges are given instructions and representations of stimuli, and computer programs require input and design. A number of scientists have worked through several options to address this tricky task. 3.1. Categorization of whistles by researchers Categorization of whistles both by humans through visual inspection of spectrograms and by computational methods produces varying results. All authors have focused on the very noticeable differences in frequency contours among dolphin whistles and have tried to create sorting systems that take contour into account. In order to accommodate contour, other parameters (e.g., duration, absolute frequency) may be ignored. Buck and Tyack (1993) emphasized contour but also designed their categorization method to be sensitive to changes in duration, a difficult task. They created a quantitative method to compare the similarities of predominant whistles and addressed the problem of time dilation by applying a dynamic time-warping technique (used with speech recognition) to align contours of different durations as long as one was not twice as long as the other. In a test of the method, the program compared extracted single-loop contours produced by five different dolphins to three new same-contour exemplars produced by each of those dolphins. In this procedure, each new exemplar was compared to all of the original models. Using confidence ratings related to distance-from-model comparisons between original models and new exemplars, all exemplars (15/15) were successfully categorized by whistler. Using the same procedure with multi-loop whistles led to correct assignment of 14/15 exemplars. In this second case, two (or possibly three) whistles could be considered upsweep/rises. All of these exemplars were appropriately categorized by whistler, a clear external indicator by which to define a category. Janik (1999) compared four methods for categorizing dolphin whistles. Humans categorized contour extractions of 104 randomly chosen whistles that were produced by four captive dolphins in the same or separate pools (Janik and Slater, 1998). Any whistle separated by a pause (including multi-loop whistles) was considered a separate whistle. Categorizers had experience analyzing bird sounds but not dolphin whistles. Instructions did not include number of animals or contexts but did emphasize the possibility of stereotyped signals. The other three methods required quantitative computer analyses. One was McCowan’s (1995) method in which 20 frequency measurements were taken at equal intervals across a whistle contour thereby eliminating duration information. Pearson product-moment correlations and k-means cluster analyses produced a maximum number

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of non-overlapping clusters in a two-dimensional representation of a k-dimensional space. Because this solution could lead to some undetected overlapping, Janik used a variation of McCowan’s technique to take overlapping into account. Janik also used two cross-correlation techniques that were sensitive to duration differences; one produced a matrix of similarity via cross-correlation coefficients, and the second produced a matrix of dissimilarity via average frequency differences taken every 5 ms between two whistle contours. These matrices were used in hierarchical cluster analyses. The results of these categorization methods differed. Human categorizers were best at categorizing whistles by whistler and context. For predominant whistles, agreement was very high (Kappa = 0.92). Humans appeared to use a gestalt sense of the overall contour shape. The computer methods focused on a variety of individual features that led to categories other than by whistler; given current data, we cannot assume that these categories have any meaning for dolphins. Later Deeke and Janik (2006) used an adaptive resonance theory (ART) neural network to categorize the same dolphin whistles analyzed by Janik (1999). The method included the use of both a dynamic time-warping technique similar to Buck and Tyack’s (1993) to be responsive to duration changes as well as an unsupervised learning algorithm which allowed evaluation of relative frequencies rather than absolute frequencies. The network’s level of critical similarity (“vigilance”) was calculated using the whistles produced by a single dolphin in isolation (i.e., one dolphin’s predominant contour). Then the network was tested at this vigilance setting with whistles produced by each of the four dolphins in isolation as well as with whistles produced by the same dolphins when they were in a group (Janik, 1999; Janik and Slater, 1998). Categorization of predominant whistles by whistler was over 90%, comparable to human sorters. Nonpredominant whistle contours were not grouped by whistler and could not be evaluated for biological relevance. In their later work, McCowan and Reiss (2001) used 60 frequency measurements distributed across contour with good agreement between computer and human categorization of whistles (Kappa = 0.82). In this case the people were given 168 whistle templates and instructed to label whistles using these templates if they found a correspondence between the sets. Whistles were not categorized by whistler; one shared whistle type, the upsweep/rise, was the most common type. Whether or not these categories are relevant to dolphins is unknown. In sorting whistles researchers have prioritized different whistle characteristics. The Caldwells (e.g., 1990) prioritized predominant whistle contours and categorized segments of whistles that could be construed to be part of a predominant whistle contour as that predominant whistle contour; they reported very high percentages of predominant individualized whistle contours. McCowan and Reiss (1995b,c, 2001) prioritized contour over duration; McCowan’s (1995) quantitative categorization technique did not reflect differences in duration. That decision may have made upsweep/rises harder to discriminate (Watwood et al., 2004). Janik (1999) prioritized the gestalt contour of whistles because it matched dolphin whistle use across contexts most closely, but he also tracked parameters like duration and small differences among contours. He evaluated the biological rel-

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evance of his categories based on the external validation of whistler as category marker. These differences in categorization schemes have affected whistle repertoire estimates and the recognition of individualized frequency contours. The Caldwells’ scheme may have led to an overestimate of the production of individualized predominant whistles versus other whistle contours. McCowan and Reiss’s analyses may have lumped upsweeps that varied in discriminable ways together. Until we have fine-tuned information about how dolphins categorize their whistles, assessments of categorization methods will be controversial. One obvious, but broad, natural category for organizing whistles is by whistler. To date, several qualitative and quantitative methods for categorizing whistles have led to whistle groupings by whistler when those whistles were whistle contours produced most often by an isolated dolphin. In some instances these same (and other) categorization schemes have resulted in categories that are not related to whistler, but we have no way of knowing whether these other groupings are relevant to dolphins. 3.2. Summary and evaluation of the existence of individualized signature whistles in dolphins As stated earlier, the signature whistle framework sets up the expectation that dolphins produce individualized contours when they are isolated and need to broadcast identity/state information. Many studies support this contention. Predominant whistles are much more commonly produced when dolphins are or appear to be outside of visual contact with each other than when they are together (Cook et al., 2004; Gish, 1979; Janik et al., 1994; Janik and Slater, 1998; Smolker et al., 1993). Antiphonal whistle exchanges are frequent when animals are separated (Gish, 1979; Lang and Smith, 1965; Sayigh et al., 1990). Some whistle exchanges include whistle matching, i.e., different dolphins will whistle the same whistle contour serially (Gish, 1979; Janik, 2000a; Tyack, 1993). In most cases this whistle is or appears to be the predominant whistle of the other dolphin in the exchange (Gish, 1979; Sayigh et al., 1990; Tyack, 1993). Although each dolphin produces an individualized contour most often when isolated, other characteristics of that whistle can change (Caldwell et al., 1990; Janik et al., 1994; Sayigh et al., 1990; Tyack, 1986). These changes may convey state information, although we have no evidence to corroborate this use of predominant whistles. Calves appear to develop these predominant contours in response to their acoustic environments (Fripp et al., 2005; Miksis et al., 2002). Contours of adults’ predominant whistles generally remain stable across many years, but male dyad partners’ whistles may influence the contours of their partners (Smolker and Pepper, 1999; Watwood et al., 2004). Whistle characteristics may reflect regional differences (Graycar, 1976), and whistle repertoires vary among social groups (McCowan and Reiss, 1995b). Male dyads share more whistle contours within dyads than between dyads (Watwood et al., 2004). Taken together, these findings suggest that whistles are learned. In addition, young dolphins’ whistles are more variable than adult whistles, and their whistle repertoire changes considerably

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across the first year (Caldwell and Caldwell, 1979; Caldwell et al., 1990; McCowan and Reiss, 1995c). However, young dolphins, like their adult counterparts, produce the upsweep/rise (McCowan and Reiss, 1995c). The upsweep/rise is produced frequently and reported across dolphin social groups (Cook et al., 2004; Dreher, 1966; Janik et al., 1994; Janik and Slater, 1998; Lang and Smith, 1965; McCowan and Reiss, 1995b, c, 2001; Smolker and Pepper, 1999; Tyack, 1986; Watwood et al., 2004). This whistle type occurs early in a dolphin’s life (McCowan and Reiss, 1995c); it is likely that it is relatively easy to produce. Although the upsweep/rise contour is very common among dolphins, no study (including McCowan and Reiss, 2001) found it to be the most commonly produced contour for every dolphin in isolation. Almost every dolphin ever recorded has produced a predominant individualized whistle contour most often when isolated (e.g., Caldwell and Caldwell, 1965, 1968; Caldwell et al., 1990; Fripp et al., 2005; Gish, 1979; Janik et al., 1994; Janik and Slater, 1998; McCowan and Reiss, 2001; Sayigh et al., 1990, 1995, 1998; Watwood et al., 2004). Sometimes that whistle contour is the upsweep/rise (McCowan and Reiss, 2001; Watwood et al., 2004). Several categorization methods have led to categorization of upsweep/rises by whistler (Buck and Tyack, 1993; McCowan and Reiss, 2001; Watwood et al., 2004). If we were to adopt McCowan and Reiss’s (2001) most recent approach and focus entirely on the upsweep/rise as the major contact call in dolphins, we could not accommodate over four decades of data in which hundreds of dolphins have been recorded and found to produce a variety of signature contours at a significant rate. We could not even accommodate McCowan and Reiss’s own data in which five dolphins produced nonupsweep/rise contours at equal or increased rates compared to upsweep/rises. On the other hand, if we continue to apply the signature whistle framework to the data, including to upsweep/rises which appear to be discriminable by whistler, then we can accommodate all findings to date. Accommodation of data is a good reason to adopt one theory over another. By this standard the signature whistle framework most readily accounts for the data. A second strength of this framework is its fit with dolphin ecology. As stated earlier, that whistles are relatively low frequency allows them to be transmitted rather long distances (Janik, 2000c). However, their fundamental frequencies often fall below the 15 kHz mark above which the dolphin’s hearing becomes more sensitive (Johnson, 1968). Therefore, unique contours and a repetitive structure would be a great asset for individual recognition across expanses. That we find this individual variation so frequently makes these whistles particularly interesting to study because it appears to be a unique adaptation to dolphins’ acclimatization to sea life (Tyack, 2000). Although it is important not to over-interpret scientific findings beyond the data, it would be a shame to overlook this system’s complexity in favor of an overly reductionist model. Of course, the final arbiter in categorization of whistles must be the dolphin (Caldwell et al., 1990; Gish, 1979; Herman and Tavolga, 1980; Janik et al., 1994; Janik and Slater, 1998; McCowan and Reiss, 1995b, 2001; Ralston and Herman, 1989;

Reiss and McCowan, 1993; Reiss et al., 1997; Sayigh et al., 1990; Tyack, 2003). 4. Acoustic perception The signature whistle framework suggests not only that dolphins learn whistles and produce individualized contours in appropriate contexts, but also that dolphins discriminate among whistles, discriminate between same-contour whistles, and associate specific contours with whistlers. This section reviews studies of the perception of narrowband sounds by dolphins. The stimuli have been both electronic and natural. Studies using natural stimuli have occurred both in labs and via playbacks to wild dolphins. 4.1. Perception of narrowband electronic sounds The earliest study requiring discrimination of electronic whistles was a communication study with two captive dolphins in California and, later, Hawaii. Whistles that were translated from human speech (mostly vowels) by two electronic translators designed for the task were projected into the water (Batteau and Markey, 1968). The dolphins received rewards for performing specific actions to the electronic whistles, e.g., touching a ball with a pectoral fin. The dolphins also received a “repeat” command and received some commands in sequence. Although the dolphins responded appropriately to many of the whistle commands, including repetition of the whistles, deciphering the outcome is difficult. Clear information on control procedures (randomization of trials, balanced schedules, cue controls) was not included in the report and may not have occurred. Later studies included much clearer controls. Among the first were two studies confirming that a dolphin can make fine frequency discriminations. A juvenile female dolphin, Kea, discriminated between pure tone and FM signals. The relative frequency difference limens (DL/F in Hz × 100) between 2 and 53 kHz were 0.2 and 0.4%, and between 53 and 130 kHz, not more than 0.8% (Herman and Arbeit, 1972; Thompson and Herman, 1975). To put this into perspective, the difference between two consecutive semitones (two keys next to each other on a piano) is about 6% (Dowling and Harwood, 1986). Kea also performed a series of cognitive tasks with acoustic stimuli. She made a series of successful reversals with a large corpus of electronically generated sounds (Herman and Arbeit, 1973). She performed a delayed-matching-to-sample two-alternative task with a large variety of 2.5-s electronically generated sound stimuli and performed almost perfectly with delays up to 2 min, the longest delay required (Herman and Gordon, 1974). When stimulus sounds were shortened to 0.2 s or less, performance fell to chance (Herman and Gordon, 1974). When only two sound stimuli were used, inter-trial intervals were reduced below 30 s long, and irrelevant sounds were played during most of the retention delay, performance accuracy dropped, suggesting interference (Herman, 1975). See Herman (1980) for a more in-depth review of this work. In another study of acoustic perception and memory, Kea heard a list of up to six 2-s within-category sounds each separated

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by 0.5-s silences and then identified whether or not a probe sound had been on the list (Thompson and Herman, 1977). Half of the probes had been on the list; a non-list (new probe) sound was from another category except with the 6-item list. There were six categories of oscillator-generated sounds: continuous frequency, frequency modulated, amplitude modulated, two different frequencies, pulsed with continuous frequency, and signals alternating between two frequencies. The dolphin performed better with short lists than long lists and remembered most recent items better than earlier items. Above-chance performance for the first item of the list occurred for lists up to four items in length. Kea also performed a conditional match in which she associated two acoustic samples with responses to specified paddle locations (Thompson and Herman, 1981) and sounds A and B with sounds C and D, respectively (Herman and Thompson, 1982). Similarly, she learned three sound–object associations; each sound led her to respond to a specific object (ball, life ring, cylinder) (Herman, 1980). In a similar but more elaborate study, another young female dolphin, Phoenix, learned more associations (Herman et al., 1984). Phoenix responded to electronically generated whistlelike sounds that were designed, with the exception of the sounds representing the two dolphins (Phoenix and Akeakamai) housed at the study site, to be different from naturally occurring dolphin whistles. Phoenix responded appropriately to at least 28 different sounds (at least 15 associated with specific objects) as well as responding differentially to multiple combinations and sequences of those sounds including those with which she had had no previous experience. Performance was analyzed in cognitive and linguistic terms; acoustic confusions were not analyzed (Ralston and Herman, 1989). There was a single exemplar of each sound that was consistent across the experiment after initial training with that sound. However, when Phoenix had trouble learning a sound, it would be changed temporarily to make it more discriminable, e.g., some sounds were lengthened in duration until they were learned and then shortened later. Others were changed permanently to make them easy to discriminate. The whistles representing the dolphins were based on their most common whistle contour, their signature whistles. Phoenix also participated in a study focusing on her ability to discriminate among electronically generated frequency contours and transfer to contours transposed to different frequencies (Ralston and Herman, 1995). Phoenix began by discriminating between flat and descending contours; each contour was created with four pure tones separated by 90 ms. Each tone in the descending contours differed from the previous tone by four semitones. Frequencies in flat and descending contours overlapped to ensure that the task could not be solved based on absolute frequency alone. The dolphin was rewarded for whistling after the descending-frequency contours and remaining silent after the flat single-tone contours. The whistle/silence response paradigm was spontaneously adopted by Phoenix who refused to perform a two-paddle response to the stimuli. She used a variety of whistles to respond to the stimuli almost none of which were her typical six-loop signature whistle.

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After the original two contours were discriminated, 13 new exemplars were gradually incorporated into the study. Performance with new stimuli varied. She only required 2 sessions to reach the 80% criterion with the fifth and sixth new contours but 16 sessions with the final two contours. Multiple analyses suggested that both absolute frequency and contour information governed her performance. A similar result occurred when the stimuli were changed such that tones in the descending stimuli were only two semitones apart and all 15 contours were presented within sessions rather than across sessions. When the stimulus pairs became descending versus ascending (rather than flat) contours (an upsweep), Phoenix’s response accuracy improved, and she responded to the frequency contours rather than to absolute frequency. Performance accuracy remained high when the contours were transposed at least a full octave above the previous stimuli. 4.2. Discrimination of whistles in the lab Phoenix and her tank mate Akeakamai also participated in a playback study in which the dolphins whistled more to computer-generated whistles that were similar to dolphin whistles than to computer-generated pulsed sounds, whistles unlike dolphins’ whistles, and sounds used in training (Bauer, Richards, and Herman, unpublished data). Occasionally, the dolphins reproduced the playback sounds. In subsequent playbacks, the dolphins produced many whistles to playbacks of Phoenix’s signature whistle, fewer whistles to computer-generated whistles, fewer still to Akeakamai’s signature whistles, and fewest to whistles of unknown dolphins. However, the dolphins whistled more after hearing all of these stimuli than they had in the monitored pre-playback period. These data suggest that the dolphins were discriminating between some whistles. In another playback study in which heartbeat was the dependent variable, a captive adult female dolphin’s heartbeats accelerated more to playbacks of a tank mate’s predominant whistle than to background tank noise (Miksis et al., 2001). The studies that produced the clearest data suggesting discrimination of conspecifics’ whistles were conducted with a wild-caught captive male estimated to be about two years old. This dolphin listened to multiple exemplars of signature whistles produced by two juvenile males recorded over 9–10 months in a variety of contexts (Caldwell et al., 1969, 1971a). Within a trial the subject heard 2–4 whistles from one of the recorded dolphins and was rewarded for pushing a paddle for one dolphin’s whistles and ignoring the whistles of the second dolphin. Trials were randomized. Numbers of trials/session were variable. The number of stimuli used in the experiment was not specified. The subject dolphin clearly discriminated between the whistles of the two dolphins that produced them; performance accuracy was above 90%. That the dolphin transferred his discrimination to new exemplars was not clear because his reinforcement history with the stimuli was not specified. Based on the number of stimuli provided and the technology used, it is likely that the dolphin did have a reinforcement history with the test stimuli before testing. For example, in one segment of the

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study there were 10 30–50-trial sessions based on 18 stimuli; clearly stimuli were re-used. Performance accuracy stayed above 80% when the stimuli were reduced to naturally occurring half- to single full loops; stimulus duration ranged from 0.03 to 0.71 s and averaged 0.29 to 0.36 s. With artificially truncated stimuli (specific information was not available; durations ranged from 0.05 to 0.51 s and averaged 0.18–0.28 s), the dolphin’s behavior became erratic and performance accuracy varied from 45 to 83%. After three of these sessions, the shortened stimuli were dropped from the study. The dolphin performed three more sessions 8, 15, and 22 days after these sessions using the original stimuli and maintained high performance accuracy. Because the signal-to-noise ratio varied in the stimuli, the dolphin’s ability to maintain discrimination across whistles presented within noise was measured; he performed very well although required a slightly longer signal when noise levels were high. The same subject performed a similar go/no-go task with whistles from four dolphins serving as negative stimuli and whistles from four other individuals serving as positive stimuli (Caldwell et al., 1971b). Stimuli were single, continuous whistles and could be multi-loop whistles if no pauses occurred. At least one whistle from each of the eight dolphins that produced stimuli for this study was presented in every session, and no specific exemplar of any whistle was presented more than once within a session. More details on session construction were not available. The dolphin pushed a paddle appropriately in response to the whistles produced by the four “positive” dolphins and did not push the paddle to the whistles produced by the four “negative” dolphins; on 100 trials, performance accuracy was over 96%. Again, reinforcement history with the stimuli was not documented, and transfer of discrimination to unfamiliar stimuli did not appear to have taken place. Therefore, the dolphin may have learned information about specific stimuli, and thus his ability to categorize new exemplars of the same dolphin’s whistle is unknown (Ralston and Herman, 1989). Similarly constructed studies suggested that a bottlenose dolphin could discriminate between whistles produced by bottlenose dolphins and other cetaceans (Caldwell et al., 1971c). 4.3. Discrimination of whistles in the wild Because dolphins produce individualized whistle contours, one major question is whether or not they recognize that a specific contour is associated with its producer. The best answers we have to this question come from playbacks of natural whistles to wild dolphins. One playback study focusing on wild dolphins compared the number of head turns each of two similarly aged offspring, independent from their mothers, made to two sets of recorded whistles (Sayigh et al., 1998). One set of whistles was produced by the mother of one of the offspring in the pair; the second set was produced by the mother of the other offspring in the pair. At the time of testing these pairs of subjects had similar rates of association with the two mothers that had produced the stimulus

whistles. Six pairs of offspring were tested. Results were analyzed by pairs. In four of the pairs there were significantly more head turns towards the predicted mothers’ whistles. For these pairs, there were a total of 153 head turns towards the predicted stimulus (an offspring’s own mother’s whistle) and 116 head turns towards the whistles of the non-related females. Similarly constructed pairs of mothers were tested in a parallel procedure. Of four tested pairs, one pair produced significantly more head turns towards the predicted stimulus (the whistles of a mother’s own independent offspring). In a second study with a design similar to the one described above, mothers and their independent offspring were tested with synthetic, computer-generated whistles that retained frequency contour information but omitted any other acoustic information, e.g., harmonics, initial attack, etc. (Janik et al., 2006). Even without this potential “voice” information, 9 of 14 dolphins turned their heads more often towards the synthetic whistles based on productions of related versus unrelated dolphins. Similarity of a subject’s own whistle to the stimuli did not appear to affect the subjects’ responses, and related individuals represented in the study did not have whistles that were more similar than those of unrelated individuals. The authors cited motivational issues as a likely explanation for the five dolphins who did not respond as predicted. The production of the data produced from these two studies required the experimenters (1) to know the histories and association indices for many wild dolphins, (2) to have high quality recordings of their mothers or offspring, (3) to be prepared to test a considerable number of dolphins due to the vagaries of capture/release opportunities, and (4) to be able to temporarily capture and restrain some of the dolphins of interest. Each dolphin participated in a 13.25-min trial of which a minute included the stimulus whistles (30 s from the related animal, 30 s from the unrelated animal). Occasionally, boat noise led to aborted trials that precluded potential subjects from being represented in the final analysis. The researchers made extensive efforts to control for familiarity of the stimuli. In this case, familiarity was tacitly defined as how often the subjects heard the whistles currently versus how often they had heard them in their lives altogether. By the nature of the relationship, each calf had likely heard its own mother’s whistle more often than other whistles and may have responded to familiarity of the whistle rather than recognition of its producer; in either case, this response suggested whistle recognition based on contour, however. In addition, because Janik et al. (2006) used computer-derived contours, the dolphins in the study could not have heard these specific whistles earlier. Therefore, that most dolphins responded as predicted suggests that they categorized new exemplars of the same dolphin’s signature whistle together. A great strength of playback studies in natural settings is that they offer opportunities to test questions of interest with untrained animals naturally responding to biologically salient stimuli. This same strength limits experimental controls. Laboratory experiments are constrained in other ways but offer opportunities for finer stimulus control that allow different sorts of questions.

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5. Vocal contextual and production learning Converging evidence from observational studies on whistle ontogeny (Fripp et al., 2005; Miksis et al., 2002; Sayigh et al., 1995), dialects (Graycar, 1976), whistle sharing (Smolker and Pepper, 1999; Watwood et al., 2004), and whistle matching (Janik, 2000a; Tyack, 1986, 1993) suggests that dolphins learn their whistles. However, in order to show that one individual learns to produce an unfamiliar contour by hearing it, one must know the learner’s original whistle repertoire (Janik and Slater, 2000). Current technology does not allow this opportunity with wild dolphins, and so studies of production learning are restricted to captive dolphins with a clearly delineated baseline repertoire. Two early studies suggested that dolphins could reproduce aspects of acoustic stimuli. In one a young male may have imitated an electronic sound (Caldwell and Caldwell, 1972). In another with three dolphin subjects, each dolphin listened to a human model produce from 1 to 10 consonant–vowel or vowel–consonant syllables (Lilly, 1965). There were 198 syllables randomly produced. Overall, the subjects produced the same number of syllables as the human models in 71% of the trials. In the clearest study showing vocal production learning by a dolphin, a five-year-old wild-caught female dolphin, Akeakamai, reproduced computer-generated whistles (Richards et al., 1984). Before the study began, she and her tank mate, Phoenix, were recorded across 14 months in a variety of contexts including undisturbed contexts. Only whistles were analyzed, and these whistles were not reported by context. Of 3401 whistles, 40.1% were Akeakamai’s signature whistle, 50.3% were Phoenix’s signature whistle, 8.1% were described as short whistles (<250 ms) or “chirps”, 1.4% were long whistles, and 0.1% were apparently imitations of artificial sounds projected into the tank for other studies. None of these sounds was used in the study. Sixteen sounds were modeled. The dolphin was rewarded for producing approximations of the sounds, hence, technically, the dolphin’s “imitations” were shaped. However, at least two or three whistles appear to have been faithfully imitated after the first attempt. In addition, the dolphin reproduced aspects of the models that were not required. Production often occurred just before the model sound ended. Reliability was tested with four sounds; the dolphin reproduced those sounds reliably. She also learned to produce five of the sounds in response to seeing five different objects. Some sounds were not produced reliably; they tended to move towards characteristics of her signature whistle (Richards, 1986). Occasionally, the dolphin transposed her responses by an octave, but, although she changed the frequency of the sounds, she maintained the frequency contour of the model in her reproductions (Richards et al., 1984). Absolute frequency was repeatedly ignored. Another study with two adult dolphins also indicated that whistle reproductions can be shaped with reinforcement. An adult male and an adult female dolphin were exposed to computer-generated whistles: a downsweep, an upsweep, and a U-shaped whistle (Sigurdson, 1993). After a long period of reinforced approximations, the male could reproduce each con-

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tour, although he could not begin the downsweeps or upsweeps at the required frequencies. The U-shaped whistle’s contour was produced very well, but it did not usually match in absolute frequency. Production of each sound had to be painstakingly trained. The female learned to produce the downsweep and the U-shaped contours. Initial responses to the downsweep occurred through autoshaping, and then instrumental conditioning techniques were applied. Eventually the U-shaped contour was presented within sessions with the downsweep model. Initially, the dolphin responded with the downsweep and then began to be silent after the U-shaped contour. After two sessions of the silent response, she spontaneously produced an approximation of the U-shaped contour. Shaping techniques led to better performance over time. Two studies suggest contextual vocal learning in dolphins. In the first, two young male dolphins, Pan and Delphi, used an in-air keyboard marked with a variety of dark grey PVC shapes that could be moved around the keyboard (Reiss and McCowan, 1993). Two adult females, the calves’ mothers, were also in the tank. The keys on the keyboard varied. The keyboard was available during 30-min sessions one or more times a day, and keyboard use was voluntary on the part of the dolphins. Pushing a specific key led to a computer-generated whistle designed to be similar to a dolphin whistle and unique to that key. After the whistle, an object or service associated with that key was distributed, i.e., a fish (although the fish key was removed apparently due to its overuse by the dolphins), a ball, a ring, and a rubdown by a person. The whistles were designed to be different from the whistles of the dolphins in the tank, but they may not have been. The baseline data concerning the dolphins’ pre-keyboard vocalizations were vague (lasting 0.3–1.5 s with frequencies from 2 to 40 kHz), but extracted whistle contours produced by the young males were available in another paper on whistle contour development (McCowan and Reiss, 1995c). Across the first year of life, Pan produced at least 24 different whistle contours, and Delphi produced at least 14 different whistle contours. Not all of the contours were distinctly different from the keyboard whistles, e.g., Delphi’s whistle type 60 was similar to the keyboard’s “ring” contour. However, whether or not the young male dolphins imitated unfamiliar whistles, the whistles they did produce immediately after hearing the keyboard models were interesting in their fidelity and lack thereof. In some cases, a dolphin reproduced absolute frequency and duration, e.g., when a dolphin produced a partial contour: the last half of the “ball” whistle. However, most whistles occurring immediately after the models maintained the frequency contour of the model but changed the absolute parameters, e.g., they had different fundamental frequencies and/or expansions or compressions in time and frequency. Reiss and McCowan (1993) also documented contextual learning, i.e., the use of an existing signal in a new context based on experience (Janik and Slater, 2000). (Janik and Slater put this learning into a social context, but it appears to apply here even though the social aspect of the context is somewhat cloudy.) During one year the dolphins’ productions of the keyboard whistles were counted and correlated with behaviors during keyboard sessions: 80% (74 whistles) of their ball whistles occurred during ball play; 73% (47 whistles) of their ring

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whistles occurred during ring play; 100% (5 whistles) of their rub whistles occurred during rubdowns; and 82% (28 whistles) of combination ring-ball whistles (each whistle produced contiguously with the other) occurred during simultaneous ring/ball play. In a somewhat similar study, six computer-generated whistles were projected into a tank with two infant male dolphins and two adult females (Hooper et al., 2006). After the projection of one of three whistles, a specific toy (ring, boatfloat, ball) associated with a specific whistle was tossed into the tank; after the projection of the other three whistles, nothing occurred. Again, a catalog of baseline whistles was not reported. As in the previous study, whistles immediately following the models included partial segments, frequency-transposed contours, and compressed or expanded contours similar to those of the models. Reproductions of whistles paired with toys occurred sooner in the study and more often than the other three whistles. Of the toy-paired whistles produced during the whistle sessions, 45–58% occurred when the dolphins were oriented towards or playing with the matched toy. 6. Signature whistle discrimination and categorization by the dolphin: a perceptual test Existing data address some of the dolphin’s acoustic perceptual abilities. Dolphins can make fine frequency discriminations (Herman and Arbeit, 1972; Thompson and Herman, 1975). They have a good memory for acoustic stimuli (Herman and Gordon, 1974; Thompson and Herman, 1977). They can associate computer-generated sounds with animate and inanimate objects as well as places and actions (Batteau and Markey, 1968; Herman, 1980; Herman et al., 1984; Herman and Thompson, 1982; Thompson and Herman, 1981). Dolphins can discriminate between a downsweep and a flat contour as well as between a downsweep and an upsweep and transfer that discrimination across octaves (Ralston and Herman, 1995). Duration is salient in discrimination of electronic whistles (Herman et al., 1984). Dolphins are sensitive to absolute frequency as well as relative frequencies (Ralston and Herman, 1995). Narrowband sounds of very short duration (0.2 s) are difficult to discriminate (Caldwell et al., 1969; Herman and Gordon, 1974). Vocal learning studies offer information about the parameters of sounds to which dolphins pay attention. Dolphins can vocally match the number of utterances they hear (Lilly, 1965). They can learn to match their whistles to a model (Richards et al., 1984; Sigurdson, 1993) and to imitate immediately, although this ability has only been documented in a few instances (Richards et al., 1984). Dolphins readily reproduce amplitude modulation but often ignore absolute frequency and duration (Reiss and McCowan, 1993; Hooper et al., 2006; Richards et al., 1984). The ends of whistles are salient, as are the contours (Hooper et al., 2006; Reiss and McCowan, 1993). Dolphins can spontaneously learn to produce a whistle in a new and appropriate context (Hooper et al., 2006; Reiss and McCowan, 1993) and can be taught to produce certain whistles in the presence of randomly chosen objects (Richards et al., 1984; Richards, 1986).

In relation to natural whistles, we know that dolphins can discriminate among whistles based on their producers (Caldwell et al., 1969, 1971b), and this discrimination does not require voice cues (Janik et al., 2006). Dolphins may associate whistles with their producers (Janik et al., 2006; Sayigh et al., 1998). Many questions concerning dolphin perception and categorization of signature whistles remain unanswered, and these questions plague researchers trying to determine a dolphin’s whistle repertoire and its potential uses (Caldwell et al., 1990; Gish, 1979; Herman and Tavolga, 1980; Janik et al., 1994; Janik and Slater, 1998; McCowan and Reiss, 1995b, 2001; Ralston and Herman, 1989; Reiss and McCowan, 1993; Reiss et al., 1997; Sayigh et al., 1990; Tyack, 2003). First, if dolphins use signature whistles to maintain contact with specific individuals, then they should be able to discriminate among a group of signature whistles and associate those whistles with their producers. To date, studies have measured essentially two responses to any set of signature whistles: head turn left or right; press the paddle or ignore the paddle (Caldwell et al., 1969, 1971b; Janik et al., 2006; Sayigh et al., 1998). One could imagine that a dolphin calf could track “Mother” and “Not Mother”, a mother could track “My Current Calf” and “Not My Current Calf”, a male dyad partner could track “My Partner” and “Not My Partner”, etc. However, dolphin social structure suggests that it is more likely that dolphins track multiple dolphin–whistle pairings simultaneously. Second, although a signature whistle’s contour essentially remains stable, its parameters can vary in many ways. These variations may contain information beyond that of identity. To use such a system, a dolphin needs both (a) to categorize new exemplars of the same whistle contour together and (b) to discriminate among same-contour whistles. Current data do not clearly show either of these abilities with natural whistles, although Janik et al.’s (2006) findings do suggest categorization of new computer-generated exemplars based on experience with natural whistle contours. Third, discrimination by whistler may be based on voice cues or contour or both. And if the dolphin does not use voice cues, as shown by Janik et al.’s findings (2006), then it is not clear if the dolphin discriminates among same-contour whistles (including the upsweep) produced by different dolphins. Determining whether a dolphin can discriminate among same-contour whistles produced by different dolphins could help us understand the role of whistle matching between dolphins. Fourth, basic questions about categorization by contour remain. For example, should scientists group partial loops that follow complete contours as being separate or as part of one utterance? Are whistles that humans find to be similar less discriminable by the dolphin? Researchers come to different conclusions when facing these questions, and they need guidance from dolphins themselves (e.g., Caldwell et al., 1990; Janik, 1999; McCowan and Reiss, 1995b; Tyack, 1986). The following questions are addressed in the current study: (1) Can a dolphin track several signature whistles at once and associate them with their producers? (2) Does a dolphin categorize new exemplars of whistles with the same contour together? (3) Can a dolphin discriminate among same-contour whistles produced by the same whistler? (4) Can a dolphin categorize whistles by the “voice” of the whistler alone? (5) How do dol-

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phins categorize the same whistle contours produced by more than one dolphin? (6) How do dolphins categorize whistles that include partial loops? (7) What whistles are more or less discriminable to a dolphin? Can they discriminate among whistles that we find to be similar? 6.1. Experiment 1 If dolphins identify whistles with whistlers, then they must be able to discriminate among whistles produced by a number of whistlers as well as to associate those whistles with their producers. This experiment was designed to determine whether a dolphin could discriminate among six different dolphins’ whistles and associate them with surrogate dolphins, i.e., different paddles/places from which the whistles originally emerged. 6.1.1. Materials and methods 6.1.1.1. Subject. The subject, Nina, was a wild-caught female dolphin (Tursiops truncatus) in her twenties housed at the Seas, Epcot® , Walt Disney World® Resort, Lake Buena Vista, FL. She was on breeding loan from the Navy’s SPAWAR organization and had previous experience in a Navy training program. She had no previous experience in a research setting. She received about a quarter of her daily fish (capelin, smelt, herring) allotment during a research session. Sessions were conducted in a small, quiet concrete tank, one of the three tanks in which Nina lived. 6.1.1.2. Stimuli. The six stimuli were whistles recorded from wild dolphins in a temporary capture/release program that was part of a long-term study of wild dolphin populations in Sarasota Bay conducted by Randy Wells and his associates (e.g., Wells, 1991, 2003). The whistles were collected and digitized by Peter Tyack and his associates from the Woods Hole Oceanographic Institution in Massachusetts. Particulars concerning whistle collection and analysis were documented

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in several articles including Sayigh et al. (1990) and Sayigh et al. (1995). Whistles were collected in air primarily using suction-cup hydrophones and recorded onto a Sony TC-D5 M, Marantz PMD-430 stereo tape recorder (frequency response of 30–15,000 Hz), or a Panasonic AG-6400 stereo hifi VCR (frequency response of 20–20,000 Hz). Some of the six dolphins who produced whistles for this study are referenced in studies of Sarasota Bay dolphins. I have included here the original numerical referents used to identify these dolphins by the researchers focusing on Sarasota Bay. However, I have also renamed each dolphin to highlight its relationships to the dolphins that produced whistles for the current study. This organization is useful because, of the six whistlers, each one is associated with another whistler in some clear way. Therefore, there are six whistlers presented in three pairs. Stimuli are identified by these names; they follow the colons in the following list and are presented in bold type. The specific whistles used in this study were produced by PAIR 1: Dolphin 22: Mother-of-Daughter and her female calf 148: Daughter; PAIR 2: Dolphin 7: Mother-of-Son and her male calf 12: Son; PAIR 3: male adult Dolphin 73: Dyad1 and his partner Dolphin 74: Dyad2. See Fig. 1 for spectrograms of the whistles. See Table 1 for spectrographic measurements for all stimuli used in Experiment 1 and Experiment 2. Digitized versions of these whistles were generously provided by Peter Tyack and his graduate students. The whistle contours represented the contours produced most often by each of the dolphins during temporary capture, i.e., the dolphins’ signature whistles. The whistles from the mother/calf pairs (Mother-ofDaughter/Daughter, Mother-of-Son/Son) were included in the analyses of Sayigh et al. (1990, 1995). In Sayigh et al. (1995), human judges rated Mother-of-Son’s (7) whistle and Son’s (12) whistle as being rather similar, 3.77, on a 5-point rating scale (1 = not similar; 5 = very similar) whereas Mother-of-Daughter’s (22) whistle and Daughter’s (148) whistle were rated as being not very similar, 1.60 on the same scale.

Table 1 Spectrographic measurements of all the whistle stimuli Frequency

Time to 1st loop max frequency

Duration

Average loop duration

Average interloop interval

# of loops

0.104 0.239

3 3 1 2 4 7

Onset

Min

Max

End

Range

Original stimuli Daughter Mother-of-Son Dyad1 Son Mother-of-Daughter Dyad2

6374 10680 8441 5771 11111 5340

5857 6460 3790 2326 7494 4910

18949 17829 14470 15676 20500 14470

18174 16538 3790 12834 11800 7580

13092 11370 10680 13351 13006 9561

0.364 0.197 0.163 0.395 0.035 0.087

1.231 1.074 1.196 0.781 0.621 1.710

0.341 0.199 1.196 0.342 0.064 0.199

New exemplars Son PS1 Dyad1 PS1 Daughter PS2 Daughter PS3 D1 imitating D2 PS1 D2 imitating D1 PS2 D1 imitating D2 PS2 D1 imitating D2 PS3

6115 6804 6546 6115 4479 8441 5426 6804

2326 5168 6546 6115 3962 6977 5426 6460

15848 14040 18605 19380 14212 10680 13695 14298

12662 5168 9388 19380 5426 6977 13006 12920

13523 8872 12059 13264 10250 3704 8269 7838

0.398 0.135 0.329 0.325 0.110 0.152 0.131 0.070

0.779 0.969 0.625 1.270 0.978 0.549 0.627 0.621

0.343 0.969 0.252 0.334 0.326 0.549 0.199 0.163

0.096 0.193 0.088 0.093 0.122 0.134 0.000 0.015 0.066

2 1 2 3 3 1 3 3

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The male dyad members (Dyad1 and Dyad2) were recognized as a dyad in Wells (1991), and their whistles were compared in Watwood et al. (2004) in which 73:Dyad1 was designated as FB26 and 74:Dyad2 was designated as FB48. This pair’s simple-ratio coefficient of association had been greater than 0.5 since at least 1982. In Watwood et al. (2004), human judges rated Dyad1’s (FB26) whistle and Dyad2’s (FB48) whistles as being rather similar, 3.68, on a 5-point rating scale (1 = not similar; 5 = very similar). However, Dyad1’s whistles were more similar to each other (4.00/5.00) as were Dyad2’s whistles (4.75/5.00). Results from a quantitative contour similarity technique (similar to that used by Smolker and Pepper, 1999; McCowan, 1995; McCowan and Reiss, 2001) were highly correlated to the results provided by human judges. 6.1.1.3. Apparatus. The response array consisted of six response paddles which were attached to the side of Nina’s tank via PVC frames. Placed at the bottom of each frame was a different object. The objects were everyday items judged to be easily discriminable. They included a white styrofoam cone, a section of a white metal gutter, a black plastic toilet float, a flat white plastic box top grid, a plastic-handled metal trowel, and a large plastic flower with white petals and a yellow center. The objects were always placed in the same positions relative to each other (from Nina’s left to right: flower, trowel, white grid, black float, gutter, styrofoam cone), therefore, the dolphin could represent the response paddles either through object identity or paddle position. See Fig. 2 for the experimental setup.

In the center of the response array was a USRD F42B transducer used as a projector (2–50kHz) amplified with a Crate PA-4+ (model #P4 + DHB0196) amplifier (system response frequency from 25 to 25000 Hz ± dB). The digitized whistles were stored and accessed via a Micron Pentium MPC P166 computer with a Dalanco Spry Model 250 Digital/Analog conversion board (sampling frequency 80 kHz). 6.1.1.4. Procedure. Training sessions, described below, were similar to test sessions. For the final 20 test sessions, the dolphin performed a conditional matching task in which each of the six signature whistles described above was uniquely associated with one of the response paddles. (For example, Daughter’s whistle was associated with Flower.) Whistle–paddle associations were randomly chosen via a random number generator. At the start of each trial, the dolphin was positioned in front of the transducer above which the trainer was sitting. To avoid inadvertent cueing, the trainer listened to white noise and was na¨ıve to the identity of the whistle. A remotely positioned research assistant played a whistle which was projected by the transducer through the system described above. The dolphin touched one of the response paddles, and the trainer advised the research assistant of the dolphin’s choice. If the dolphin chose the paddle associated with the whistle that was played, the trainer blew her bridge (a pure tone used as a secondary reinforcer), and the dolphin received two smelt. If the dolphin chose incorrectly, she was summoned back to the transducer for the next trial. Each whistle was presented three times within each session. Order of whistle presentation was randomized.

Fig. 2. The experimental setup. The dolphin is positioned underwater in front of a transducer that projects the whistle stimuli. Response paddles are differentiated by underwater objects and are always in the same places. The trainer is na¨ıve to the identity of the whistles and identifies the dolphin’s choice. A technician uses the computer to play the whistles and records the dolphin’s choices.

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Before the final test trials, training and periodic testing occurred concurrently. Training was conducted as described in the last paragraph except that the dolphin was cued via sound location for whistles she had not yet learned to associate with their specified paddles. In this case, not only did the whistle emerge from the center transducer, but it also emerged from a second transducer (same models) located behind the appropriate paddle. All paddles had transducers or facsimiles of transducers located behind them. Occasionally, the dolphin was tested without the second localization-cue transducer. When she could correctly choose the appropriate paddle without the localization cue for 3/3 trials in three consecutive sessions, the second transducer was silent on those trials thereafter, and the dolphin had to choose the paddle without the help of the localization cue. Through the use of these localization cues, the whistles essentially issued from the paddles. In addition to localization cues, correction trials were also used during training. If the dolphin missed a trial, it was repeated. If she chose correctly within two correction trials, she was rewarded with a single smelt. If not, she was cued by hand to the appropriate response in a final correction trial. Correction trials did not occur during test sessions and were not included in the results. 6.1.2. Results and discussion The dolphin was able to discriminate among the six whistle stimuli. In the last 20 18-trial sessions the dolphin’s performance accuracy averaged 86.39 % (311/360, S.D. = 10.27%) and was clearly above-chance levels of 17% in this six-alternative task (binomial, p < 0.0001). See Fig. 3 for performance accuracy in the last 20 test sessions. Some whistles were learned more quickly than others. If the dolphin chose the correct paddle after hearing the whistle associated with that paddle for 3/3 uncued trials in three consecutive

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Table 2 The number of trials required by the dolphin to reach the criterion (3/3 correct choices in three consecutive sessions) for each whistle–paddle pair Whistle

Trials to criterion

Daughter Mother-of-Son Dyad1 Son Mother-of-Daughter Dyad2

1068 1875 675 819 1443 876

sessions, then the dolphin had met the criterion for learning that whistle–paddle association. The dolphin learned to touch the appropriate paddle for Dyad1’s whistle after 675 trials but only learned to touch the appropriate paddle for Mother-of-Son’s whistle after 1875 trials. See Table 2 for number of trials to criterion for all paddle–whistle pairs. Although the dolphin did not often choose incorrectly in the final 20 sessions, she did have one notable confusion. She incorrectly chose Daughter’s paddle after hearing Mother-of-Son’s whistle 14 times (23.33%), and she incorrectly chose Mother-ofSon’s paddle after hearing Daughter’s whistle 8 times (13.33%). See Table 3 for a confusion matrix illustrating the dolphin’s choices in the final 20 sessions. These paddles were next to each other, and paddles did not change locations. Therefore, the confusion could have been place-based, but this option seems unlikely given that there were no other place-based confusions. The dolphin was probably confusing the whistles themselves. Mother/male calf whistles (Mother-of-Son/Son) and Dyad members’ whistles may be perceived as being similar by humans and dolphins (Sayigh et al., 1990, 1995; Watwood et al., 2004), but the dolphin in this experiment did not confuse them. The whistles she did confuse, Mother-of-Son and Daughter, were more similar to each other in minimum frequency, maximum

Fig. 3. Performance accuracy in identifying the six whistles in the final 20 18-trial sessions. The line indicates chance performance of 17%.

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Table 3 The frequency of the dolphin’s choices after the presentation of each original whistle stimulus Choices

D’ter

M-of-Son

Dyad1

Son

M-of-D’ter

Dyad2

No resp

Whistles D’ter M-of-Son Dyad1 Son M-of-D’ter Dyad2

46 14 0 0 2 0

8 41 0 1 1 1

1 1 59 1 0 0

0 0 0 58 0 1

1 4 0 0 54 3

4 0 0 0 2 53

0 0 1 0 1 2

The far left column indicates the projected whistle, and the top row indicates the chosen paddle. The final column indicates no choice.

frequency, end frequency, and number of loops than to other stimuli. Their contours were more similar to each other than to most of the other contours, although Son’s contour was also similar to these two contours. In summary, this experiment confirms that dolphins can discriminate among a group of six signature whistles and associate each whistle with “its producer”. This ability is necessary if dolphins use whistles to track a group of dolphins. However, the dolphin only experienced a single exemplar of each dolphin’s whistle in this experiment. Although this design was chosen in order to avoid training the dolphin to group multiple whistles by the same whistler together, it also made it possible for the subject to use artifacts in the stimuli in order to make the discrimination (Kroodsma et al., 2001). The next experiment addressed both the potential issue of artifacts in the original stimuli as well as dolphin categorization of whistles by whistler through the presentation of unfamiliar exemplars. 6.2. Experiment 2 In this study the subject experienced new exemplars produced by a subset of the whistlers from Experiment 1. Some of the new whistles were produced by the whistlers that normally produced them, and some of the whistles were reproductions produced by the dolphins in the male dyad whistling each other’s preferred contours. All of the whistles were naturally occurring variations; however, some preserved the original frequency contours better than did others. The use of these new whistles as stimuli supported several goals. First, the subject’s categorization of whistles by whistler could be explored. Secondly, the subject’s use of vocal characteristics of the whistler for this categorization was examined both through the inclusion of new exemplars as well as apparently imitated whistles. If the subject used the “voice” of the whistler to classify whistles, then she should be able to classify new exemplars with their whistler and she should associate an imitation with the whistler. On the other hand, if the subject associated a contour with the dolphin that normally produced it, then categorization should be affected by contour distortions and, for reproduced whistles, the subject should choose the paddle linked to the whistle’s potential referent. Finally, the new exemplars served as a control for Experiment 1. Although the whistles used in Experiment 1 were recorded with suction-cup hydrophones in air and should have had high signal-to-noise ratios as well as similar sound artifacts, it is possible that any

specific whistle may have included identifiable sound artifacts. Expected categorization of unfamiliar stimuli would suggest that the subject had not been using artifacts in Experiment 1. 6.2.1. Materials and methods 6.2.1.1. Subject. The subject was the same subject that participated in Experiment 1. 6.2.1.2. Stimuli. The stimuli used in this experiment included both new whistles and those used in Experiment 1. All stimuli came from the same source, the Tyack/Wells collaboration in Sarasota Bay. New stimuli were different exemplars of the signature whistles produced by the same dolphins described earlier. Half of the whistles were apparent reproductions of one dolphin’s contour produced by a second dolphin, the dyad members. See Fig. 4 for spectrograms of the eight new whistles and Table 1 for spectrographic measurements of all stimuli. The new stimuli were randomly grouped into three sets. Probe Set 1 included a new exemplar of Son’s whistle, a new exemplar of Dyad1’s whistle, and an apparent reproduction of Dyad2’s contour produced by Dyad1. Probe Set 2 included a new exemplar of Daughter’s whistle, Dyad1 reproducing Dyad2’s contour, and Dyad2 reproducing Dyad1’s contour. Probe Set 3 included yet another new exemplar of Daughter’s whistle, Dyad1 reproducing Dyad2’s contour, and, as a check for reliability, the same exemplar used in Set 1 of Dyad1’s whistle. 6.2.1.3. Procedure. The procedure was the same as that outlined in Experiment 1 except that before the experiment began the dolphin did not receive a fish reward on one pre-designated trial in each session irrespective of her paddle choice for 20 consecutive sessions. After 20 sessions with pseudo-randomly chosen unreinforced trials, new whistles were inserted as probes in each session. One probe was included in each 18-trial session and presented to the dolphin 12 times. The dolphin was never reinforced for a probe trial. Probe trials were organized into three sets. Each set included 3 whistles and required 36 sessions until completion. The order of presentation of probe whistles was randomized across sessions, although an equal number of probes for each whistle occurred as the first, second, and third presentations of that whistle contour within a session. The reader should note that although Experiment 2 is presented after Experiment 1, Experiment 1 had not been completed before Experiment 2 began. Due to unexpected circumstances

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261

Fig. 4. Spectrograms illustrating the frequency contours of the probe stimuli. Frequency is on the vertical axis and time is on the horizontal access. The left column contains new exemplars of similar contours produced by the original whistlers. The right column contains reproductions of whistle contours by and of the male dyad members.

the dolphin subject was recalled by the Navy. Therefore, it was not clear that there would be enough time for the dolphin to learn to discriminate all six whistles before her return. For that reason, Experiment 2 was conducted when the dolphin had learned to choose reliably only four of the six paddles associated with each whistle. All paddles remained in the water for all sessions and the dolphin heard all six original stimuli in each session, but the dolphin still experienced localization cues for Motherof-Daughter’s and Mother-of-Son’s whistles. New exemplars of these dolphins’ whistles were not tested. Although all paddles were available during exemplar testing, and the dolphin chose 5/6 of the paddles (as well as not responding on occasion), chance performance for all analyses was conservatively set at

25% due to the localization cues at the two paddles associated with Mother-of-Daughter and Mother-of-Son. Average performance accuracy for the four learned whistle–paddle associations for the final 10 sessions (12 trials/session without the inclusion of the results associated with whistles produced by Mother-of-Daughter and Mother-of-Son) before the introduction of probes was 97.5% (117/120), clearly above-chance performance of 25% (binomial, p < 0.0001). 6.2.2. Results and discussion The dolphin chose the paddles associated with the whistler for each new exemplar whistle that was not a reproduction 25 out of 48 times (52.01%), a level significantly above a chance level of

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Table 4 The dolphin’s choices with the probes: new exemplars produced by original whistlers and reproductions of whistles of and by dyad males Choices

Daughter

Mother-of-Son

Dyad1

Son

Mother-of-D’ter

Dyad2

No resp.

Exemplars Son PS1 Dyad1 PS1 Daughter PS2 Daughter PS3 Dyad1 PS1 repeat 3

3 2 1 11 1

0 0 0 0 0

1 7 9 0 8

6 1 1 0 2

1 0 1 0 0

1 2 0 0 1

0 0 0 1 0

Reproductions D1 IM D2 PS1 D2 IM D1 PS2 D1 IM D2 PS2 D1 IM D2 PS3

3 8 11 11

0 0 0 0

4 4 1 0

2 0 0 0

1 0 0 1

1 0 0 0

1 0 0 0

Each probe was presented 12 times at the rate of one per session. Predicted choices are in bold. Spectrograms of whistles are available in Fig. 4. “PS” refers to the set in which each exemplar was presented.

25% (binomial, p < 0.0001). Performance accuracy was much higher with the three whistles (Son PS1, Dyad1 PS1, Daughter PS3) that had intact contours, 24/36 (66.67%), than with the whistle contour (Daughter PS2) that was not intact, 1/12 (8.33%). See Table 4 for the dolphin’s choices with all new stimuli presented in Experiment 2. The dolphin was never reinforced for responses to these exemplars. In the event that she adopted a lose-shift strategy after receiving no reinforcement for these whistles after repeated presentations, an analysis of her first six paddle choices (the first half) for these exemplars was conducted. She chose the paddle associated with the whistler less often for the last six (the last half) presentations of the new exemplars than for the first six presentations. In the first half she chose the paddle associated with the whistler 15/24 times (62.5%) when including the partial-contour whistle and 15/18 times (83.33%) without the partial-contour whistle. In the second half she chose the paddle associated with the whistler 9/24 times (37.5%) when including the partial-contour whistle and 3/18 times (16.67%) without the partial-contour whistle. However, over Experiment 2 as a whole she did continue to choose the paddle associated with the whistler when new exemplars were presented; Dyad1’s new exemplar whistle was presented both in the first group of probes, and, as a re-check, in the last group. In the first set of presentations, she chose Dyad1’s paddle after his whistle 7/12 times, and in the second set she chose Dyad1’s paddle after his whistle 8/12 times. Apparently, lack of reinforcement did not drive her performance entirely. In the eight trials in which each unfamiliar whistle stimulus was presented for the first time, the dolphin subject refused to choose any paddle 2 (25%) times. This refusal coupled with her reduced performance accuracy with new exemplars compared to original whistles even though she apparently identified most of them (all but the partial-contour one) suggests that the dolphin recognized that the new exemplars were different from the original whistles. It is unlikely that the difference was related to background artifacts in the sound files because one would not expect differential performance with partial- and intact-contour stimuli due to artifacts; artifacts are not likely to be consistently different in one group and not the other. In addition, that the

dolphin categorized 83.33% of the new intact exemplars with the whistler in the first half of the probes and only 16.67% of the new intact exemplars with the whistler in the second half of the probes suggests that she recognized similarities in contour (83.33%) as well as recognizing differences that led to unreinforced responses (16.67%). These data are the only data in the literature confirming that dolphins can differentiate among different utterances by the same whistler. This discrimination is necessary for receivers if they are to use the differences in whistle characteristics (e.g., absolute frequencies, whistle rates, etc.) that often occur in signature whistles to gain information about whistlers beyond their identity. For example, these differences could broadcast the emotional state of the whistler (Caldwell et al., 1990) and lead to differential responses from listening conspecifics. When presented with apparent reproductions of whistles by and of the dyad members, the dolphin subject chose the paddles associated with the dyad members fairly infrequently, 10/48 (20.83%) times, which was not above-chance levels of 25% (binomial, p = 0.316). In the first six trials with each reproduction, performance accuracy was better: 44.44%, 8/18 times (Dyad1’s paddle 7 times, Dyad2’s paddle 1 time—the only time she ever chose Dyad2’s paddle with the reproductions) but not significantly above a chance level of 25% (binomial, p = 0.057). The dolphin was more likely to choose the expected paddles with new exemplars than with reproductions, χ2 (1, N = 96) = 8.81, p < 0.005. However, three of the new-exemplar contours were clearly intact (all but Daughter PS2) whereas three reproduction contours included partial whistles (all but Dyad1 IM Dyad2 PS1). Therefore, another perspective on performance is available. If one groups probe whistles with intact contours together (Son PS1, Dyad1 PS1, Daughter PS3, Dyad1 IM Dyad2 PS1) and whistles with partial contours together (Daughter PS2, Dyad1 IM Dyad2 PS2, Dyad2 IM Dyad1 PS2, Dyad1 IM Dyad2 PS3), a comparison shows that expected choices are more likely to occur following whistles with intact contours (29/48, 60.42%) than with partial contours (6/48, 12.5%), χ2 (1, N = 96) = 21.41, p < 0.0005. A comparison of responses to Daughter’s (PS3) intact exemplar, 11/12, versus to Daughter’s (PS2) partial-contour exemplar, 1/12, highlight this tendency.

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Fig. 5. Percentage of choices the dolphin made after hearing each probe. The four bars on the left illustrate choices after an intact-contour exemplar; the four bars on the right illustrate choices after a partial-contour exemplar. The patterns underneath the whistle titles on the horizontal axis portray the pattern associated with that whistle. For example, diagonal bars are associated with Daughter; Daughter’s paddle was chosen over 90% of the time when the intact-contour exemplar was presented (first column of intact-contour exemplars) but less than 10% of the time when the partial-contour exemplar was presented (first column of partial-contour exemplars).

See Fig. 5 for the distribution of choices the dolphin made for each new probe. Because the dolphin was trained with single exemplars of each whistle, she was not trained to categorize by contour. But she did. However, there is one potential caveat about the training here. The stimuli were chosen based on standard definitions of signature whistles including multi-loop whistles (Buck and Tyack, 1993; Caldwell and Caldwell, 1979; Sayigh et al., 2007). With the exception of Dyad1, all of the stimuli were multi-loop whistles, i.e., whistles separated by short and consistent durations. One might argue that these multi-loop whistles biased the dolphin to categorize by contour; however, her categorization of Dyad1’s (PS1) intact-contour unfamiliar exemplar was 58.33%, similar to the average of 60.42% with intact-contour unfamiliar exemplars. In addition, Dyad2’s terminal loop was somewhat distinctive in terms of contour compared to the other loops in his multi-loop whistle. (See Fig. 1 for whistle contours.) Although some researchers have suggested that dolphins treat whistles that include partial segments of signature contours similarly to whistles that include only full contours (e.g., Caldwell et al., 1990), the current data suggest that dolphins do not group such whistles together. On the other hand, dolphins with knowledge of another dolphin’s normal whistle variations may categorize these partial segments with the dolphin that produced them (Caldwell et al., 1990). The fact that the dolphin did not categorize partial contours with their producer suggests that the dolphin did not use production (“voice”) characteristics to categorize whistles. One would expect these characteristics to be available whether contour was intact or not. Of course, voice characteristics may be encoded

in high-frequency harmonics which were not available in these recordings, or they may have been available but not salient in these short clips. However, if voice cues were available and detected, contour was more salient. 7. General discussion The major focus of this study was to investigate the dolphin’s representation of whistle contour in order to determine whether the dolphin would respond in a manner that was consistent with the signature whistle framework for individual recognition in dolphins. As stated earlier, this theory of individual recognition by whistle contour implies that (1) each dolphin has a unique whistle contour, the signature whistle, that it whistles frequently when the dolphin is separated from its social group, (2) dolphins use signature whistles in contexts in which they need to broadcast identity/state information, and, at least in the main, other whistles do not broadcast identity information, (3) dolphins learn their signature whistles, (4) dolphins can discriminate among a group of dolphins’ signature whistles, (5) dolphins can both group same-contour whistles together and discriminate among same-contour whistles produced by one dolphin, and (6) dolphins can associate signature whistles with specific whistlers. Whistle production data support the first three points. First, a dolphin separated from its social group predominantly produces an individualized whistle contour (Gish, 1979; Janik et al., 1994; Janik and Slater, 1998; Sayigh et al., 1990; Sayigh et al., 2007; Smolker et al., 1993; Watwood et al., 2005). Second, dolphins appear to use these individualized contours in contexts in which they need to advertise identity (when they are out of visual con-

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tact with their social groups) and produce these contours much less often in contexts in which they are together and do not need to confirm their locations or those of others (Cook et al., 2004; Janik and Slater, 1998; McCowan and Reiss, 1995b, 2001; Sayigh et al., 1990; Watwood et al., 2005). That other whistles may also perform this function is much less clear, but it may be possible. However, antiphonal calling using signature whistles (Gish, 1979; Lang and Smith, 1965; Sayigh et al., 1990), signature whistle matching (Gish, 1979; Tyack, 1986, 1993), the ease of human and quantitative categorization of signature whistles by whistler as opposed to other whistle types (Deeke and Janik, 2006; Janik, 1999), as well as contextual use, together suggest a special and potentially unique function for this whistle type. Third, a constellation of data on the development and variety of signature whistle contours suggests that dolphins learn their whistles (Fripp et al., 2005; Graycar, 1976; Miksis et al., 2002; Watwood et al., 2004). Contour learning is relevant because it facilitates the development of calves’ signature contours that are particularly discriminable in their long-term social groups (Fripp et al., 2005; Sayigh et al., 1995) and provides flexibility for social group changes across time, e.g., the formation and reformation of male dyads (Watwood et al., 2004) as well as mother–calf pairs across births (Sayigh et al., 1995). Laboratory experiments have confirmed that dolphins can learn to produce whistles in appropriate circumstances (Reiss and McCowan, 1993) and through imitation (Richards et al., 1984). The literature on whistle production has advanced more quickly than the literature on whistle perception, and this study was designed to address some of these omissions through the use of stimuli reflecting multiple dolphins’ natural signature whistles that had to be associated with specific surrogate producers from among a group of producers. In addition, because the dolphin was trained with single exemplars of each signature whistle, i.e., the dolphin was not trained to categorize by contour, the study allowed for categorization of whistles by contour, voice cues, or other parameters salient to the dolphin. The inclusion of new intact-contour and partial-contour exemplars allowed the dolphin to use any of these categorization devices. The dolphin subject provided data that addressed several previously unanswered questions concerning dolphin perception of signature whistles. The dolphin tracked several whistles at once and associated them with their surrogate producers; she was good at it (M = 86%, chance = 17%). Previous data have confirmed discrimination of natural whistles produced by pairs of dolphins (Caldwell et al., 1969, 1971a; Sayigh et al., 1998), but none have demonstrated discrimination of a group of dolphins’ natural whistles. This discrimination is important if dolphins are to use these whistles to identify multiple conspecifics during the same time period (versus serially, e.g., My Current Dyad Partner). In addition, these are the clearest data showing association of whistles with their producers, and the only data showing association of whistles across a group of producers. Sayigh et al.’s (1998) carefully designed study with offspring/mother dolphins and their whistles suggested recognition of familiar whistle contours ostensibly associated with producers, but, of course, Sayigh could not place specific (unresponsive) dolphins to be used as response “paddles”. Although this laboratory situation

is clearly artificial, the ability to associate a natural whistle with a producer is necessary for the use of signature whistles as identifiers for individuals. These data show that a dolphin can make this association with arbitrarily chosen producers (object/place). Equally important is the fact that the dolphin continued to maintain this association when new intact-contour exemplars produced by the same whistler were presented. The dolphin categorized new intact-contour exemplars during the first half of their presentations (before lack of reinforcement appeared to affect performance) with the expected surrogate producers 83% of the time. This ability has never been demonstrated with natural whistles with a known reinforcement history. Although dolphins have shown a facility with artificial sound–object associations, no study included multiple exemplars of the sounds (Herman, 1980; Herman et al., 1984; Herman and Thompson, 1982; Thompson and Herman, 1981). In pair-wise discriminations of natural whistles, the Caldwell et al. (1969, 1971a,b) used multiple exemplars but may have reinforced choices during training. Janik et al. (2006) showed whistle recognition of computer-generated contours with wild dolphins; these exemplars had to be unfamiliar in that they were computer-generated. The findings presented here correspond to those of Janik et al. both in recognition of new exemplars of known whistle contours and in contour-based categorization. That the dolphin categorized new intact-contour exemplars by producer (60%) and did not categorize partial-contour exemplars by producer (12%) suggests contour-based categorization. Given that the definition of a signature whistle requires this sort of categorization scheme, that multiple studies of whistle production have suggested it (Gish, 1979; Janik et al., 1994; Janik and Slater, 1998; Sayigh et al., 1990; Smolker et al., 1993; Watwood et al., 2005), and that the only whistles that have been consistently categorized by producer (the only externally valid category in which we can be confident at present) using human sorters and computational methods have been sorted by contour (Buck and Tyack, 1993; Deeke and Janik, 2006; Janik, 1999), this finding is both in line with previous work and important within the signature whistle framework. This categorization occurred without multiple-exemplar training: The dolphin was not trained to categorize by contour; it happened naturally. In addition, the dolphin did not categorize partial-contour whistles with intact-contour whistles suggesting that nonsignature whistles are different from signature whistles. If signature whistles are special because they are individual identifiers, then non-signature whistles should not generally be particularly good identifiers: If any whistle will do, the signature whistle appears irrelevant. For the dolphin subject, it does not appear that any whistle will identify a surrogate producer; only an intact-contour signature whistle will do that job. To date, these are the only perception data that show this difference in categorization. This claim would be stronger if we could have presented a larger variety of producer-specific whistles to the dolphin. Partial-contour signature whistles are categorized as signature whistles by some researchers (e.g., Caldwell et al., 1990) and not by others (e.g., McCowan and Reiss, 1995b,c; McCowan and Reiss, 2001). The current data suggest that partial-contour whistles are not the same. (Deeke and Janik, 2006, also imply

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that this may be the case based on categorization of whistles by a neural network.) When it comes to partial contours of signature whistles, whistle researchers may want to be splitters. The current data also suggest that the dolphin did not categorize by voice cues—presumably either because they were absent or because they were not salient. Not only did the dolphin subject group intact-contour whistles together, but over presentations with no reinforcement (first half: 83%, second half: 17%), she began to try other responses to these different exemplars of the original whistles. This change in performance suggests that she recognized that these exemplars were different than the originals. If dolphins use differences between different exemplars of the same dolphin’s signature whistle, then they must be sensitive to these differences. To date, these are the only data showing this sensitivity to differences among intact-contour signature whistles produced by the same dolphin. In future work, researchers should look for differential responses to the same dolphin’s signature whistles to determine what information, if any, these differences might carry. This study shed no light on representation of apparent imitations of whistles. The dolphin’s performance with these whistles was ambiguous, possibly because most reproductions included partial contours. The question of how dolphins do represent these whistles is important to our understanding of the functions of signature whistles. Because dolphins can discriminate whistle contours that vary slightly and those that do not vary in contour at all, perhaps there are subtle markers on whistles that allow identification by whistler. For example, when Spray produced Scotty’s signature whistle, Spray’s version had more amplitude modulation than did Scotty’s (Tyack, 1986). On the other hand, perhaps context information is enough. For example, perhaps signature whistle matching only occurs between pairs of dolphins. In that case, identification between the pair would not be an issue. This area warrants a good deal more work. Many researchers have measured similarity between whistles using human sorters and/or computational methods (McCowan and Reiss, 1995a,b,c, 2001; Sayigh et al., 1995; Smolker and Pepper, 1999; Watwood et al., 2004). Some of the whistles used in this study were considered to be quite similar by humans; however, the dolphin did not confuse whistles that humans had rated as being similar, although humans would probably find the whistles the dolphin did confuse to be similar. The most confusions among standard stimuli occurred between Daughter and Mother-of-Son which were most similar (compared to other stimuli) in minimum frequency, maximum frequency, end frequency, and number of loops. Categorizations of unfamiliar exemplars were not predicted by frequency measurements. The number of loops may have influenced choices, although Daughter’s truncated PS2 whistle had two loops and was most often (9/12) associated with Dyad1’s single-loop whistle rather than Son, a two-loop whistle. Daughter and Mother-of-Son had somewhat similar contours as did Son. When to classify a contour as an upsweep/rise is not always clear, but by some accounts it may be that these three whistles are upsweep/rises. If that is the case, all were discriminable, although Mother-of-Son and Daughter were less so. Given the limited ways in which contours can vary, that dolphins can discriminate apparently similar whistles pro-

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duced by different dolphins is another indication that signature whistles can be useful identifiers. From the perspective of the signature whistle framework, the dolphin fulfilled the whistle perception requirements. She discriminated among a group of whistles, associated them with surrogate producers, grouped new exemplars of the same dolphin’s whistle together and discriminated among same-contour whistles produced by the same dolphin. Of course, that a dolphin can do these things does not mean that the signature whistle framework is correct; however, it does mean that it could be correct. Future studies should investigate whistle function and categorization both for signature whistles and for other whistle contours. Of particular interest would be more definitive data on a dolphin’s identification of other dolphins based on their signature whistles. The method used here was fairly non-coercive in directing the dolphin’s categorizations and allowed for analysis of confusions among a group of whistles. Clearly, by losing the subject Nina we missed opportunities to test her with more refined stimuli in which parameters and contours were varied to determine more specific delineations between categories. Later studies should address influences of duration, frequency, and amplitude modulation on dolphins’ perception of whistles as well as when one contour becomes indistinguishable from another. Nina has provided information about a dolphin’s abilities to categorize whistles, but we still know little about the mechanisms underlying that categorization. A major area of whistle perception that remains opaque concerns whistles which are produced simultaneously with clicks or burst pulses. Dolphins often overlay these vocalizations, but we know nothing about the factors that motivate these productions or how they are perceived. We also know very little about how whistle sequences and contextual use affect perception. Happily for researchers who, like Ron Weisman, enjoy the study of acoustic perception in animals, there is plenty of opportunity for future work with dolphins. Acknowledgements This article is in honor of the contributions of Ron Weisman to the study of auditory cognition in animals. This work was supported by grants from the Walt Disney World® Resort, New College of Florida, and the University of South Florida. I would also like to thank many others who helped to support this work: for dolphin training: Mark Barringer and Kim Odell as well as Cathy Goonen-Brantley, Jane Capobianco, Bobbie Cavanaugh, Conrad Litz, Tom Morris, Mike Muraco; for research coordination and on-going support: DruAnn Clark, Erika Putman, Wendi Fellner, Carrie DeLong; for stimuli, Peter Tyack and his lab including Laela Sayigh, Deborah Fripp, Kelly Jaakkola, Jennifer Miksis; for equipment help, Tony Paolero at USRD, Ed Ericsson; for help with figures: Lily Ericsson; for administrative support: Tom Hopkins, Hank Robitaille, Beth Stevens, Jane Davis, Andy Stamper; for discussions and direction: Jim Ralston, Herb Roitblat, Mark Xitco, Gordon Bauer, Wendi Fellner, Peter Tyack, John Gory, Michelle Barton, Vincent Janik, and an anonymous reviewer; for star power, Nina.

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