VOCAL INDIVIDUALITY OF IN-AIR WEDDELL SEAL (LEPTONYCHOTES WEDDELLII) PUP \"PRIMARY\" CALLS

$Page 1: VOCAL INDIVIDUALITY OF IN-AIR WEDDELL SEAL (LEPTONYCHOTES WEDDELLII) PUP \"PRIMARY\" CALLS$
MARINE MAMMAL SCIENCE, 22(4): 933–951 (October 2006)C© 2006 by the Society for Marine MammalogyDOI: 10.1111/j.1748-7692.2006.00074.x

VOCAL INDIVIDUALITY OF IN-AIR WEDDELLSEAL (LEPTONYCHOTES WEDDELLII ) PUP

“PRIMARY” CALLSKYM T. COLLINS

Australian Marine Mammal Research Centre,Zoological Parks Board of NSW,

P.O. Box 20, Mosman, New South Wales 2088, Australiaand

Faculty of Veterinary Science, University of Sydney,JD Stewart Building B01, New South Wales 2006, Australia

E-mail: kym [email protected]

JOHN M. TERHUNE

Department of Biology,University of New Brunswick,

P.O. Box 5050, Saint John, New Brunswick E2L 4L5, Canada

TRACEY L. ROGERS

Australian Marine Mammal Research Centre,Zoological Parks Board of NSW,

P.O. Box 20, Mosman, New South Wales 2088, Australiaand

Faculty of Veterinary Science, University of Sydney,JD Stewart Building B01, New South Wales 2006, Australia

KATHRYN E. WHEATLEY

Antarctic Wildlife Research Unit,School of Zoology, University of Tasmania,

Private Bag 5, Hobart, Tasmania 7001, Australia

ROBERT G. HARCOURT

Marine Mammal Research Group,Graduate School of the Environment, Macquarie University,

North Ryde, New South Wales 2109, Australia

ABSTRACT

As a result of selective pressures faced during lactation, vocal recognition mayplay a crucial role in maintaining the phocid mother–pup bond during the periodof dependence. To investigate this possibility, we examined whether Weddell seal(Leptonychotes weddellii) pups produce individually distinctive “primary” calls. Onetemporal, nine fundamental frequency features, and two spectral characteristicswere measured. A discriminant function analysis (DFA) of 15 Vestfold Hills pups

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934 MARINE MAMMAL SCIENCE, VOL. 22, NO. 4, 2006

correctly classified 52% of calls, while the cross-validation procedure classified 29%of calls to the correct pup. A second DFA of 10 known-age McMurdo Sound pupscorrectly classified 44% of “test” calls. For novel calls, the probabilities of attainingsuch classification rates by chance are low. The relationship between age and callstereotypy indicated that pups 2 wk and older may be more vocally distinctive.Overall, findings suggest that Weddell seal pup “primary” calls are moderatelydistinctive and only exhibit sufficient stereotypy to aid maternal recognition byapproximately two weeks of age.

Key words: vocal individuality, pup calls, Weddell seal, Leptonychotes weddellii.

In pinnipeds, mothers and pups are frequently separated as a result of periodicmaternal foraging at sea, disruptive social interactions, and increased pup indepen-dence throughout lactation. Subsequent pair reunions are critical to pup survivalas, in otariid and the majority of phocid species (exception: Hawaiian monk seals,Monachus schauinslandi), mothers typically nurse only their own pups (Stirling 1975).Reunions may depend upon one or both pair members and may involve multiplesenses (predominately audition, olfaction, and vision; Insley et al. 2003). Mothersroutinely use olfaction and vision to confirm pup identity at close range (Kovacs1987, Insley 1992). Conversely, acoustic cues are most effective over large distancesand are important for mother–pup reunion in all well-studied pinniped species (Insleyet al. 2003). Social recognition based on vocalizations requires individually distinctivecalls characterized by relatively low variation within individuals and relatively highvariation among them (Falls 1982). This can be achieved in various ways, e.g., vocal-izations within individuals may be variable yet still distinctive if they are sufficientlydifferent from those of other individuals (Miller 1982).

Mother–pup vocal recognition has been studied extensively in otariids and mutualrecognition appears to be characteristic of this family (Insley et al. 2003). Selectivepressures faced by otariids during breeding are likely to have resulted in the need foractive involvement by both pair members. A number of phocids experience similarselective pressures, such as moderate-to-large breeding colonies (Riedman 1990) andtemporary mother–pup separations during lactation (e.g., Kovacs 1995, Sato et al.2002) and may, therefore, also be expected to rely on vocal identity cues duringreunions. Previous investigations of northern elephant seals (Mirounga angustirostris)have demonstrated individually distinctive calls by mothers and pups (Insley 1992),and maternal recognition of pup calls (Petrinovich 1974). Furthermore, previousstudies have reported individually distinctive pup calls in harbor, Phoca vitulina(Renouf 1984), Hawaiian monk ( Job et al. 1995), gray, Halichoerus grypus (Caudronet al. 1998), and harp, Pagophilus groenlandicus (van Opzeeland and van Parijs 2004)seals.

Weddell seals (Leptonychotes weddellii) form moderate-sized colonies during thebreeding season (Stirling 1969) and undergo temporary mother–pup separations(Hindell et al. 2002, Sato et al. 2002) during the 5–7-wk lactation period (Lugg1966, Tedman and Bryden 1979, Riedman 1990, Siniff 1991). During the first2 wk post-partum mothers use olfaction and vision to reunite with pups over shortdistances (Tedman and Bryden 1979). However, during the second half of the nursingperiod, pup movements into and out of the water become less synchronized with theirmothers’ activities (Tedman and Bryden 1979). Such increased pup independence,combined with the mothers’ inconsistent attendance during this period (Hindell

COLLINS ET AL.: INDIVIDUALITY OF WEDDELL SEAL PUP CALLS 935

et al. 2002, Sato et al. 2002), is likely to necessitate reunions during which acousticcues would be the most effective means of communication. Previous studies haveconfirmed that mothers and pups counter-call during reunions and that maternalcalls are individually distinctive (Kaufman et al. 1975, Collins et al. 2005: referredto as “contact” calls). These findings suggest that pups may indeed play an activerole during reunions, through the production and possible recognition of distinctivein-air mother–pup “primary” calls.

The present study investigated the hypothesis that Weddell seal pups produceindividually distinctive “primary” calls by examining: (1) individuality of acousticcharacteristics, (2) discrimination among individuals, and (3) the relationship be-tween age and call stereotypy. Pup “primary” calls (PPCs) are emitted with openmouths and consist of a fundamental frequency with associated harmonics, variablein number and strength.

METHODS

In the Vestfold Hills (VH), breeding colonies contain up to 35–50 mother–puppairs (Tedman and Bryden 1979, McFarlane 1996), with numbers generally averagingaround 10–20 pairs per colony (Pahl et al. 1997). In contrast, the McMurdo Sound(MS) colonies sampled, Turtle Rock and Hutton Cliffs, contain as many as 50–100mother–pup pairs (Siniff et al. 1977). The densities of such colonies have been shownto vary throughout the summer, with minimal nearest-neighbor distances rangingfrom approximately 2.4 to 9.6 m during pupping (Stirling 1969, Kaufman et al.1975). As peak pupping in the VH occurs from early October to early November(Lugg 1966), individuals included in the VH analysis may range from newborn pupsup to 3–4 wk of age. Conversely, the MS analysis was performed on known-ageindividuals.

DATA COLLECTION

Vestfold Hills

Recordings were collected in November 1997 from four breeding sites: WeddellArm (WA), Partizan Island (PI), Long Fjord (LF), and Topografov Island (TI), nearDavis Station, Antarctica (68◦31.9′S, 78◦11.5′E). Calls were recorded between 1200and 2400 during periods of low wind and no precipitation. Actively vocalizing sealswere recorded for longer periods compared with seals emitting few calls. Using afrontal approach to alert the animals before close contact was established, the singleresearcher approached mother–pup pairs while they were hauled out or swimmingin a pool (Terhune et al. 1993). The microphone was then brought within 3 m ofthe seal’s throat or mouth with the researcher indicating verbally that the focal pup,its mother, or a distant seal produced the call recorded. Jaw snaps (associated withaggressive behavior by the mother, Terhune et al. 1993) were directed towards theresearcher only, while mother–pup “primary” calls were produced when pair memberswere orientated towards each other, the researcher, or conspecifics. Recording sessionswere terminated if the pup began to nurse, the adult females became aggressive(i.e., lunged toward the researcher or produced jaw snaps), or the seals began tomove away from the researcher. Seals were not tagged during the current study;however, 12 of the 15 mothers bore unique tags from previous research (Green et al.1995).


Procedures were approved by the Antarctic Science Advisory Committee (projectnumber 2122). Disturbance to the animals was minimized by approaching individualcolonies only once a day for less than 6 h (including data collection for other projects),and no more than 2 d in a row. Individual colonies were visited one to four timesduring the study period.

McMurdo Sound

Recordings were collected from October to December 2003 from three breedingsites: Turtle Rock, North Hutton Cliffs, and South Hutton Cliffs, near McMurdoStation, Antarctica (77◦51′S, 166◦40′E). Calls were recorded between 0800 and 2200during periods of low to moderate wind and no precipitation. As all pups in MS aretagged within 3 d of birth, and all tags at breeding colonies are read every 3–5 d(Cameron and Siniff 2004), seals are likely habituated to close approach by researchscientists. The equipment box was positioned within 5 m of the focal mother–puppair and left to record for 90 min. The video footage recorded (in the absence of aresearcher) revealed vocal behavior similar to that observed in the VH, with mother–pup “primary” calls produced while pair members were oriented towards each otheror conspecifics. The footage was used to determine whether the focal pup, its mother,or a distant seal produced the call recorded. Tag numbers were noted at the time ofrecording. The exact age of the pup, if known, was also noted at this time. If an exactage was not known the researcher estimated the pup’s age based on its tag number,as all pups were sequentially tagged throughout the field season and birth dates wereknown for approximately half the colony. There was a possible error in the estimatedage of 2–3 d.

Data collection was conducted under authorities from the Animal Ethics Com-mittees of Macquarie University (Animal Research Authority AEC 2002/009),the University of Tasmania (Animal Ethics Committee project number A6790),and the Department of Conservation, New Zealand (Marine Mammal PermitPer/17/2003/188).

RECORDING EQUIPMENT

VH recordings were made using a hand-held Sennheiser ME66 microphone (0.05–20 kHz ± 2.5 dB) fitted with an MZW 20 windscreen and a Sony DAT TCD-D7 taperecorder (0.02–20 kHz ± 1.0 dB). MS calls were recorded using a Sennheiser ME66microphone fitted with a Rycote Softie windsock and a Sony DAT TCD-D8 taperecorder (0.02–20 kHz ± 1 dB). Video footage was recorded using a Sony Digital8DCRTRV355 Handycam with TDK P5-90HMPPEN Hi8 tapes. The MS equipmentwas housed within an insulated box, containing heat packs, with the video cameralens and microphone projecting externally. The box was anchored to the fast ice withice screws.

ACOUSTIC ANALYSIS

PPCs included in the analyses were positively identified as being produced bythe focal individual, and exhibited good signal-to-noise ratios. These requirementscombined with field logistics limited our two data sets. The VH data set included15 replicate calls from each of 15 pups (e.g., Fig. 1). Four additional calls appeared


Figure 1. Spectrograms representing three replicate “primary” calls from Vestfold HillsWeddell seal pups (a) 2, (b) 3, (c) 4, and (d) 8.

to be variants and were not included in the analyses. The MS data set included 12replicate calls from each of 10 known-age pups. The vocalizations of each individualwere collected during a single recording session. Calls were digitized at a samplerate of 12,500 Hz and analyzed as spectrograms (bandwidth 0–5,000 Hz, FFT 512data points, analyzing bandwidth 24.4 Hz) using SIGNAL 3.1 (Engineering Design,Belmont, MA) (Fig. 2). The following 12 acoustic characteristics were measured:

(1) Duration of call (DUR),(2) Minimum frequency of fundamental (f 0) (MINF),(3) Maximum frequency of f 0 (MAXF),(4) Start frequency of f 0 (STARTF),(5) First-quarter frequency of f 0 (1/4F),(6) Second-quarter frequency of f 0 (2/4F),(7) Third-quarter frequency of f 0 (3/4F),(8) End frequency of f 0 (ENDF),(9) Mean frequency of f 0 (defined below) (MEANF),

(10) Coefficient of frequency modulation of f 0 (defined below) (CoFM),(11) Numeric value of the harmonic band displaying maximum energy (MAXE1),

and(12) Numeric value of the three harmonic bands of maximum energy (MAXE1-2-3).

The accuracy of the graphics cursor measurements (VH: time: ±7.1 ms, frequency:±21.6 Hz; MS: time ± 8.9 ms, frequency: ±21.6 Hz) was determined by monitorsettings used to display the spectrograms.


Figure 2. A spectrogram of a Weddell seal pup “primary” call (FFT 512, analyzing band-width 24.4 Hz). Note: In this example ENDF and MINF occur at the same point, however,this is not always the case. See text for definitions of terms.

Frequency characteristics (2)–(8) were measured from the fundamental frequencyusing the spectral contour as a guide. This SIGNAL function derives the contourby detecting the frequency maximum at each time column along the fundamentalfrequency. The first eight acoustic characteristics were measured directly from thespectrograms using the graphics cursor. Additional frequency measurements werethen taken at successive 1/10 increments along the fundamental’s total durationbetween STARTF (0/10) and ENDF (10/10). These 11 measurements were then usedto calculate MEANF, and CoFM using the formula:

CoFM =t = n − 1∑

t = 1

(abs( ft − ft + 1))/(n − 1), divided by MEANF × 100,

where abs denotes the absolute value, ft represents the frequency at time t, and nis equal to the number of sampling points (Harrington 1989, Collins et al. 2005).CoFM was used as a measure of standardized frequency modulation (i.e., calculatedas the average rate of frequency modulation relative to the mean frequency of the


fundamental). Spectral characteristics (11) and (12) were measured by displayingpower spectra of the entire time signal. The numeric value of the three harmonicbands displaying maximum energy (e.g., fundamental = 1, first harmonic = 2) werethen noted ( Job et al. 1995, Charrier et al. 2003). MAXE1-2-3 measurements weregrouped irrespective of the ordering of the bands into maximum energy 1, 2, and3. For example, Group 1 included all of the following possible combinations: 1-2-3,1-3-2, 2-1-3, 2-3-1, 3-1-2, and 3-2-1.

STATISTICAL ANALYSIS

Calls produced successively may be more acoustically similar to each other than callsthat are well spaced in time (Miller 1979). To address this possibility, we investigatedthe relationship between call similarity and inter-call interval (based on the VH dataset) using PRIMER 5 (PRIMER-E Ltd., Plymouth, PL). For each VH pup, thevalues of acoustic characteristics (1)–(11) were simultaneously compared betweenevery possible pair of replicate calls (n = 105). For example, pair-wise comparisonsamong three replicate calls would include the following comparisons: 1 vs. 2, 1 vs. 3,and 2 vs. 3. The resulting measures of pair-wise call similarity, calculated for all pups,ranged from 67% to 99%. Corresponding inter-call intervals were also calculatedand ranged from 1 to 624 s. Linear regressions revealed a significant relationshipbetween call similarity and inter-call interval for pups 6 and 12 only (r > −0.23,P < 0.02). However, the slope of the regression lines established that less than 8%of the variation in call similarity was explained by inter-call interval.

Individuality of Acoustic Characteristics

Based on the VH data set, within-individual (CVi) and between-individual (CVb)coefficients of variation were calculated for continuous characteristics (1)–(10) usingthe formula for small samples:

CV ={

100

(SD

xmean

) (1 + 1

4n

)},

where n is the population sample (Sokal and Rohlf 1995, Charrier et al. 2002). Eachcharacteristic’s potential for individual coding (PIC) was then assessed by calculat-ing the ratio CVb/mean CVi, where mean CVi is the mean value of the CVi of allindividuals (Robisson et al. 1993, Charrier et al. 2002).

Discrimination Among Individuals

The potential for discrimination among individual VH pups, based on the contin-uous characteristics, was investigated by performing discriminant function analysis(DFA) using STATISTICA 6 (StatSoft, Inc., Tulsa, OK). To fulfill the normalityassumption of a DFA, DUR and CoFM were square-root transformed while the re-maining frequency characteristics were log2-transformed (converting frequency datainto octaves). DFA also requires that individual characteristics included in the analysisexplain at least 1% of the data’s variance. If any characteristic violates this require-ment the data set will be termed “ill conditioned” and the analysis will not proceed.Although a number of the characteristics included in the analysis were correlated,this assumption was not violated.


First, a DFA was performed on the entire VH data set (n = 225 calls) to deter-mine which acoustic characteristics discriminate among the calls of individual pups( Johnson and Wichern 1992). Second, to establish an unbiased estimate of the num-bers of calls correctly classified to individuals a more conservative cross-validatedDFA was performed ( Johnson and Wichern 1992). The cross-validation procedurerequired the data set to be divided into two groups: (1) a “training” data set consist-ing of 10 replicates from each pup, and (2) a “test” (novel) data set containing theremaining five replicates for each pup. The “training” data set (n = 150) was used tocalculate the discriminant functions that were, in turn, used to classify the “test” calls(n = 75). The classification values calculated were dependent upon which replicateswere analyzed as “test” calls. Consequently, three separate DFAs were performed toensure that each replicate call was analyzed as novel data once. The resulting threesets of classification values were then averaged (Collins et al. 2005). Using a bino-mial distribution we calculated: (1) the probability of achieving this average level ofdiscrimination, or greater, by chance, and on an individual level (2) the minimumnumber of correctly classified calls required to be statistically significant (P < 0.05).

The potential of the categorical spectral characteristics [(11) and (12)] to discrim-inate among VH pups was investigated using ordinal logistic regression, performedin MINITAB 14.1 (Minitab Inc., U.K.). The analysis of MAXE1-2-3 was performedon five groups that included all combinations of harmonic bands: (1) 1-2-3, (2) 1-2-4,(3) 1-2-5, (4) 1-2-6, and (5) Other (1-2-7, 1-2-8, 1-2-9, 1-3-4, 1-3-5, 1-4-6, 2-3-4,2-3-5, and 2-3-6). To reduce data complexity Group 5 incorporated nine combina-tions that occurred relatively infrequently. A significant result was further investi-gated through rotation of the reference category (i.e., pup 1, 2, etc.), and examinationof the logistic regression table to identify the individuals between whom significantdifferences occurred.

Age and Call Stereotypy

The DFA performed on the entire MS data set included analysis of 120 PPCs. Toperform the cross-validation procedure the data set was divided into two groups: (1)a “training” data set consisting of eight replicate calls from each of the 10 pups (n =80), and (2) a “test” data set containing the remaining four replicates for each pup(n = 40). The resulting three sets of classification values were averaged. The numbersof calls correctly classified to each pup were then compared with the pup’s age.

RESULTS

INDIVIDUALITY OF ACOUSTIC CHARACTERISTICS

PIC values for characteristics (1)–(10) were greater than 1 (Table 1), with call DURexhibiting the highest potential for individuality. Conversely, STARTF and CoFMwere quite variable within individuals, producing relatively low PIC values comparedwith the remaining frequency characteristics measured.

DISCRIMINATION AMONG INDIVIDUALS

The DFA on the entire VH data set revealed a significant difference among pups(Wilks’ � = 0.06, F(140,1,666) = 5.00, P < 0.01). Three roots of the DFA identified


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Table 2. Three DFA roots identified the dominant characteristics used to discriminateamong the “primary” calls of 15 Vestfold Hills Weddell seal pups.

Acoustic characteristic Root 1 Root 2 Root 3

DUR −0.57 0.81 0.33MINF −0.12 0.10 −0.28MAXF 0.08 0.09 0.28STARTF −0.13 −0.24 0.311/4F −0.04 −0.16 −0.482/4F 0.46 0.39 −0.423/4F −0.24 −0.42 −0.44ENDF 0.38 −0.41 1.11MEANF 0.61 0.70 0.34CoFM 0.13 −0.25 −0.15

Eigenvalue 2.30 0.82 0.65Cumulative proportion 0.52 0.71 0.86

A characteristic was reported to be a dominant feature when the absolute value of its rootwas greater than 0.50 (in bold).

three dominant characteristics used by the analysis to discriminate among individuals(Table 2). A characteristic was identified as a dominant feature when the absolute ofits DFA root value was greater than 0.50. Differences in DUR and MEANF valuesamong pups accounted for the majority of acoustic variation explained by Roots 1 and2 (71%). Furthermore, ENDF accounted for the greater part of an additional 15%of the data’s variance (Root 3). The DFA performed on the entire data set classified52% of calls to the correct pup.

The cross-validated DFAs revealed that, on average, 29% of the “test” calls wereassigned to the correct pup (Table 3). The probability of correctly classifying thisnumber, or greater, of novel calls by chance is low (P < 0.01). Correctly classifyingfour or more calls to an individual was significant (P < 0.05). This statistical cut-offindicates that seven pups did not produce individually distinctive PPCs (classificationvalues: 7%–20%), while eight pups demonstrated vocal individuality (classificationvalues: 27%–73%). Consistent call misclassifications (≥4) in all but one instancewere between pups from different colonies.

Ordinal logistic regression of the categorical characteristics demonstrated a signif-icant difference among VH pups (� 2 = 51.84, df = 14, P < 0.01; � 2 = 38.02, df =14, P < 0.01, respectively). However, rotation of the reference category establishedthat the pattern of harmonic bands in which MAXE1 was placed was not individuallydistinctive, with the patterns of 14 pups not significantly different (P > 0.05) fromthose of 6 to 12 other individuals (Fig. 3a). The exception was pup 6 who exhibiteda pattern statistically similar to only three other pups (pups 2, 3, and 14). Similarly,the observed MAXE1-2-3 combinations of 13 pups were not significantly differentfrom those of 11 to 13 other individuals (Fig. 3b). In this instance, the two exceptionswere pups 3 and 8 who displayed energy distributions that were statistically similarto four (pups 2, 8, 9, 14) and one (pup 3) other pup, respectively.

AGE AND CALL STEREOTYPY

The DFA on the entire MS data set classified 67% of calls to the correct pup,while the cross-validation procedure revealed that, on average, 44% of the “test”


Table 3. The average level of discrimination achieved by the cross-validated DFAs (n =15 for each pup) of the “primary” calls of 15 Vestfold Hills Weddell seal pups.

Average percentage of calls Total number of callsColony Pup (VH) correctly classified (%) correctly classified

WA 1 20 3WA 2 73 11∗

WA 3 13 2PI 4 27 4∗

PI 5 33 5∗

PI 6 33 5∗

LF 7 13 2LF 8 47 7∗

TI 9 13 2TI 10 13 2TI 11 47 7∗

TI 12 27 4∗

WA 13 53 8∗

WA 14 7 1WA 15 20 3

Average 29 Total 66/225

∗Significant (P < 0.05) (in bold).

calls were assigned to the correct pup (Table 4). For novel calls, the probabilityof correctly classifying this percentage, or greater, by chance alone is improbable(P < 0.01). Once more, correctly classifying four or more calls to an individualwas significant (P < 0.05). This statistical cut-off indicates that three pups did notproduce individually distinctive calls (classification values: 8%–25%), while sevenpups demonstrated vocal individuality (classification values: 42%–83%). The pupsthat were not found to be vocally distinctive were the three youngest pups aged ∼8,12, and 13 d.

DISCUSSION

Results indicate that Weddell seal pups produce moderately distinctive “primary”calls, with approximately one third of vocalizations assigned to the correct individual.Although this classification rate is low relative to those of otariids pups (Insley 1992,Fernandez-Juricic et al. 1999, Phillips and Stirling 2000), it is significantly higherthan expected by chance. However, individual classification rates varied widely, withcorresponding age data suggesting that Weddell seal “primary” calls only exhibitsufficient stereotypy to aid maternal recognition by approximately two weeks of age.

The most reliable acoustic indicators of identity, among a variety of mammals,appear to be features of the fundamental frequency as well as the distribution ofspectral energy (e.g., pinnipeds: Insley 1992, Job et al. 1995, McCulloch et al. 1999,Charrier et al. 2002; other mammals: Amazonian manatees, Trichechus inunguis, Sousa-Lima et al. 2002; baboons, Papio hamadrayas ursinus, Rendall 2003). “Primary” callsproduced by Weddell seal pups, like those of mothers (Collins et al. 2005), exhibit in-dividuality of fundamental frequency characteristics. In addition, the distinctivenessof call duration is consistent with results for Hawaiian monk ( Job et al. 1995), gray


Figure 3. The observed distribution of (a) MAXE1 and (b) MAXE1-2-3 among the“primary” calls of 15 Vestfold Hills Weddell seal pups.

(Caudron et al. 1998, McCulloch et al. 1999) and harbor (Khan 2004) seal pups. Incontrast, spectral call characteristics were not found to vary greatly among individ-uals. Although this finding corresponds with our analysis of Weddell seal maternalcalls (Collins et al. 2005), it does not reflect previous phocid studies that describe sig-nificant differences in peak energy distribution among pups (Perry and Renouf 1988,Insley 1992, Job et al. 1995, Caudron et al. 1998, van Opzeeland and van Parijs 2004).However, varying results between the current analysis and those of Insley’s (1992)study may be due to the fact that the latter investigation measured “formant-like”energy concentrations rather than harmonics of maximum energy.

A comparison of vocal individuality among phocid species reveals varying degreesof stereotypy that correspond to maternal recognition abilities in the species tested to


Table 4. The average level of discrimination achieved by the cross-validated DFAs (n =12 for each pup) of the “primary” calls of 10 known-age McMurdo Sound Weddell seal pups.

Average percentage of calls Total number of callsPup (MS) Age (d) correctly classified (%) correctly classified

1 ∼8 8 12 12 8 13 13 25 34 ∼14 75 9∗

5 19 50 6∗

6 21 83 10∗

7 21 42 5∗

8 ∼32 58 7∗

9 32 50 6∗

10 38 42 5∗

Average 44 Total 53/120

∼Estimated age (possible deviation of 2–3 d).∗Significant (P < 0.05) (in bold).

date (Table 5). In addition, although direct comparisons among studies are difficult(Beecher 1989, Bee et al. 2001, Insley et al. 2003), variations in maternal and breedingstrategies appear to relate to the level of call stereotypy reported. The percentage ofcalls correctly classified for Weddell, gray, harbor, and northern elephant seal pupsare comparable, and likely reflect selective pressures faced during breeding (Table 5).Harbor and gray seal mothers, like Weddell seal females, periodically return to seaduring lactation requiring pair reunions upon return to the breeding aggregation(Renouf et al. 1983, Caudron et al. 1998, Hindell et al. 2002). Equally, disruptivesocial interactions typical of large, high-density northern elephant seal colonies leadto temporary pair separations and increased risk of injury to pups (Petrinovich 1974,Riedman and Le Boeuf 1982). Conversely, Hawaiian monk seals breed in low-densityaggregations and frequently foster non-filial pups without incurring a reproductivecost (Boness 1990). Such breeding behaviors, combined with the relatively low levelof acoustic stereotypy and lack of maternal recognition reported, are indicative of anapparent lack of selection for mother–pup recognition in this species.

Nevertheless, direct comparisons of call stereotypy among studies should be as-sessed with caution; as such values can be influenced by features of the statisticaland acoustic analyses as well as the data collection methods. The fact that samplesize influences DFA classification rates has been previously highlighted by a numberof researchers (Beecher 1989, Bee et al. 2001, Insley et al. 2003). Bee et al.’s (2001)analyses suggest that the percentage of calls correctly classified by a DFA increasesas (1) the number of individuals decreases and (2) the number of replicate calls perindividual increases. Furthermore, this study indicates that the cross-validation tech-nique used (i.e., n − 1 or training/test data sets) may also alter the classification ratecalculated. In addition, Khan’s (2004) investigation of vocal individuality indicatesthat the acoustic characteristics included in an analysis can influence the degree ofstereotypy reported. In this study, a DFA performed on features of the dominantfrequency correctly classified 29% of harbor seal pup calls, while a DFA on funda-mental frequency characteristics classified 48% of calls to the correct pup. Although


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the two analyses involved different samples sizes, which may also have contributed tothe varying statistical outcomes, the importance of fundamental frequency featuresin the discrimination of individuals has been widely demonstrated (e.g., Tooze et al.1990, Scherrer and Wilkinson 1993, Caudron et al. 1998, Phillips and Stirling 2000).Moreover, the behavioral context in which vocalizations are recorded has been shownto influence an individual’s arousal state and, in turn, affect multiple acoustic features(Owings and Virginia 1978, Perry and Renouf 1988, Miller and Job 1992, Schraderand Todt 1993). Consequently, data collection across a range of arousal states mayresult in greater within-individual variation in call structure and subsequently lowerthe percentage of calls correctly classified by a DFA.

The current DFA analysis (based on an equal number of replicate calls per indi-vidual) indicated that the degree of vocal stereotypy varied widely among Weddellseal pups, suggesting that individuality might be influenced by additional biologicalfactor(s). Although seven VH pups produced classification rates that were not signif-icantly greater than predicted by chance, four of the eight distinctive pups producedrates comparable to values frequently reported as signifying vocal individuality ina number of species [60% in Mexican free-tailed bats, Tadarida brasiliensis mexicana(Gelfand and McCracken 1986); 75% in timber wolves, Canis lupus (Tooze et al. 1990);51% in South American fur seal, Arctocephalus australis, pups (Phillips and Stirling2000); and 60% in Arctic foxes, Alopex lagopus (Frommolt et al. 2003)]. Althougharousal state changes within individuals cannot be discounted, the MS analysis in-dicated that pup age may have influenced the level of Weddell seal call stereotypycalculated. Examination of the numbers of calls correctly classified revealed that thevocalizations of older pups were more easily discriminated than those emitted bypups less than 14 d of age. A similar finding of increased stereotypy with age hasbeen reported previously for two phocid species, Hawaiian monk ( Job et al. 1995)and harbor (Khan 2004) seal pups.

Investigations of offspring vocal stereotypy report that distinct calls typically de-velop with increasing offspring age and mobility, initiating the establishment of vo-cal recognition before parent–offspring separations are expected (e.g., Lenhardt 1977,Beecher et al. 1981, McArthur 1982, Jones et al. 1991, Phillips 1998, Charrier et al.2003). Weddell seal mothers aggressively maintain individual haul-out spaces dur-ing their first week post-partum and almost continually attend their pups before theyfirst enter the water (Thomas and DeMaster 1983). Such maternal behaviors ensurethat olfactory, visual, and spatial cues are sufficient to maintain the filial bond duringthis initial “critical” period (Kaufman et al. 1975, Tedman and Bryden 1979). It isplausible, therefore, that pups do not produce individually distinctive calls imme-diately after birth, yet develop distinctive calls during the first 2 wk of life beforematernal foraging trips (Hindell et al. 2002, Sato et al. 2002), increased colony den-sity (Thomas and DeMaster 1983), and increased pup independence (Tedman andBryden 1979), select for a functioning mother–pup vocal recognition system.

In summary, our overall findings suggest that Weddell seal pups produce moder-ately distinctive “primary” calls, exhibiting a lower potential for vocal individualitywhen compared with mothers (Collins et al. 2005). Nevertheless, results indicate thatby approximately two weeks of age pup calls exhibit sufficient stereotypy to allowboth mothers and pups to play active roles during reunions through the productionof vocal identity cues. However, the existence of a vocal recognition system can onlybe confirmed through playback studies verifying that mother–pup “primary” callsare indeed recognized by their intended recipient.


ACKNOWLEDGMENTS

We thank the Australian Antarctic Division and the Natural Sciences and EngineeringResearch Council of Canada for providing logistical and financial support for the Davis Sta-tion fieldwork, Tara Cheesman for collecting most of the Weddell seal recordings, and the1997 Davis researchers and staff for their field assistance. Thanks also to Aurora Expeditions,University of Sydney, PADI Aware Foundation, the Ecological Society of Australia, and theLinnean Society of NSW for providing financial support, and to Sony Australia and TDKAustralia for providing product sponsorship. The MS study was supported by Antarctica NewZealand, the SeaWorld Research and Rescue Foundation, the Australian Research Council, andthe Graduate School of the Environment, Macquarie University. The research was conductedunder the auspices of Dr. Lloyd Davis, University of Otago with support from Ailsa Hall,Corey Bradshaw, and Mark Hindell. We also sincerely thank Paul Brewin, Peter Isherwood,Sharon Mackie, Anna Harrison, and volunteers from Scott Base for assistance in the field. Weare grateful to Dr. Fred Harrington for providing corrections to the previously misprintedCoFM formula. Thanks also to Dr. John Buck and Dr. Will Uther for statistical assistance,Sophie Hall-Aspland and Brett Hill for equipment design assistance, Dr. Isabelle Charrier,Dr. Stephen Insley and reviewers for this journal for their constructive comments on an earlierdraft of this manuscript, and Joy Tripovich for the helpful discussion of ideas.

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Received: 10 August 2005Accepted: 1 April 2006

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VOCAL INDIVIDUALITY OF IN-AIR WEDDELL SEAL (LEPTONYCHOTES WEDDELLII) PUP \"PRIMARY\" CALLS