Repetition patterns in Weddell seal (Leptonychotes weddellii ...

Repetition patterns in Weddell seal (Leptonychotes weddellii) underwater multiple element calls Hilary B. Moors and John M. Terhunea) Department of Biology, University of New Brunswick, P.O. Box 5050, Saint John, New Brunswick, E2L 4L5, Canada

共Received 5 November 2003; revised 10 April 2004; accepted 29 April 2004兲 Many vocalizations produced by Weddell seals 共Leptonychotes weddellii兲 are made up of repeated individual distinct sounds 共elements兲. Patterning of multiple element calls was examined during the breeding season at Casey and Davis, Antarctica. Element and interval durations were measured from 405 calls all ⬎3 elements in length. The duration of the calls (22⫾16.6 s) did not seem to vary with an increasing number of elements (F 4,404⫽1.83,p⫽0.122) because element and interval durations decreased as the number of elements within a call increased. Underwater vocalizations showed seven distinct timing patterns of increasing, decreasing, or constant element and interval durations throughout the calls. One call type occurred with six rhythm patterns, although the majority exhibited only two rhythms. Some call types also displayed steady frequency changes as they progressed. Weddell seal multiple element calls are rhythmically repeated and thus the durations of the elements and intervals within a call occur in a regular manner. Rhythmical repetition used during vocal communication likely enhances the probability of a call being detected and has important implications for the extent to which the seals can successfully transmit information over long distances and during times of high level background noise. © 2004 American Institute of Physics. 关DOI: 10.1121/1.1763956兴 PACS numbers: 43.80.Ka, 43.80.Ef 关WWA兴

Pages: 1261–1270

I. INTRODUCTION

B. Masking and anti-masking strategies

A. Weddell seal vocalizations

Seals are able to hear under water with a maximum sensitivity between 2 kHz and 32 kHz, although the overall hearing range is from 0.1 to 64 kHz. Vocalizations that seals emit span this range 共Richardson, 1995兲. Although Weddell seal hearing abilities have never been examined, they are not expected to be substantially different from the hearing abilities of seals tested so far 共Terhune and Turnbull, 1995兲. Masking occurs when noise interferes with the ability of an animal 共seal兲 to detect a sound even when the signal is above the animal’s absolute hearing threshold 共Richardson, 1995兲. Masking of seal calls will occur when a high level of background noise, abiotic or biotic, is encountered 共Hawkins and Myrberg, 1983; Terhune and Ronald, 1986; Richardson, 1995兲. When vocalizing at large breeding sites, Weddell seals face the problem of masking due to overlapping calls of conspecifics 共Thomas and Kuechle, 1982兲. At low calling rates, individual seal calls are typically distinct, but at high calling rates, calls tend to overlap each other almost continuously. At high calling rates, background noise produced by conspecifics limits the detection range of individual seal calls 共Terhune and Ronald, 1986兲. Certain characteristics of seal calls, such as frequency separation 共Terhune, 1999; Serrano and Terhune, 2002兲, abrupt onset and offset of calls 共Watkins and Schevill, 1979; Serrano and Terhune, 2002兲, and increasing repetition of call elements 共Watkins and Schevill, 1979; Terhune et al., 1994; Serrano and Terhune, 2001兲, likely decrease the effect of masking and enhance the detection of individual calls.

Weddell seals 共Leptonychotes weddellii兲 have a circumpolar distribution around Antarctica and surrounding islands 共Bertram, 1940兲. The females gather in small breeding groups on land-fast ice in early October, and pups are born from mid-October to mid-November 共Kooyman, 1981兲. Mating occurs shortly after the pups are weaned 共Kooyman, 1981; Thomas and Kuechle, 1982兲. Male Weddell seals establish territories below the ice near the pupping colonies and spend most of their time defending territorial boundaries until mating occurs 共Kooyman, 1981兲. Weddell seals have an extensive vocal repertoire 共Thomas and Kuechle, 1982; Thomas et al., 1988; Pahl et al., 1997; Abgrall et al., 2003兲. Many call types have been described and the repertoire exhibits geographic variation between different areas along the coastline 共Thomas et al., 1988, Abgrall et al., 2003兲. These vocalizations play an important role in social communication 共Thomas et al., 1988兲. The seals appear to use sound in connection with their breeding behavior 共Ray, 1967兲, and underwater vocalizations are frequently emitted near colonies 共Kooyman, 1981兲. Territorial males are vocal underwater prior to and during the mating period 共Thomas et al., 1988兲, and some calls types, such as trills, are thought to be made only by males 共Thomas and Kuechle, 1982; Oetelaar et al., 2003兲. All vocalizations decrease sharply after the breeding season 共Thomas et al., 1987; Green and Burton, 1988兲. a兲

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J. Acoust. Soc. Am. 116 (2), August 2004

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C. Repetition in vocalizations

An element is defined as a single distinct sound having a beginning and end that are clearly distinguishable from background noise. Thus, multiple element calls consist of more than one discrete sound. The repetition of call elements in underwater vocalizations would allow calls to stand out from background noise and avoid being masked 共Watkins and Schevill, 1979兲. A regular sequence of brief sounds is more detectable against background noise than a single brief sound 共Richardson, 1995兲. Multiple element Weddell seal calls that were overlapped by the call of another seal were found to be longer 共due to the addition of elements兲 than were similar calls emitted without overlap 共Terhune et al., 1994兲. Similarly, harp seals 共Pagophilus groenlandicus兲 increase the number of elements within multiple element calls when the number of calls per minute increases 共Serrano and Terhune, 2001兲. Regular pulse repetition enhances acoustical detection thresholds for harbor seals 共Phoca vitulina兲, demonstrating that seals who repeat short duration calls at regular rates enhance the probability of communicating with distant conspecifics in both masked and unmasked situations 共Turnbull and Terhune, 1993兲. Three distinct timing patterns 共rhythms兲 in which elements of the calls occur at regular intervals have been described for harp seal multiple element calls 共Moors and Terhune, 2003兲. Repetition patterns within calls have also been described in arthropods, frogs, birds, and other mammals 共Alexander, 1968; Sebok, 1968; Lengagne et al., 1999; Pavan et al., 2000; Pollack, 2000; Schwartz , 2002; Wollerman and Wiley, 2002兲. D. Objectives

In situations when background noise levels are high and/or variable, multiple element calls will be discernable if they fit a regular pattern that distinguishes them from random sounds or other seal calls having a different rhythm pattern. Some Weddell seal multiple element calls appear to have constant element and interval durations while others appear to have consistently increasing or decreasing element and interval durations throughout the calls 共Thomas and Kuechle, 1982; Thomas et al., 1988兲. This apparent stability of the timing in calls has not yet been measured. If constant timing was found within calls, as well as between calls, it would suggest that the seals produce rhythmically repeated vocalization patterns that could potentially increase the probability of call detection by distant conspecifics. Our purpose in this study was to investigate the apparent stability of rhythms that occur in Weddell seal multiple element underwater calls and to determine if the element and interval durations, and frequencies within a call, follow consistent and regular patterns throughout the call. II. MATERIALS AND METHODS A. Recordings

Digital audio tape 共DAT兲 recordings of Weddell seal underwater vocalizations were obtained near Weddell seal breeding groups during the 1997 breeding season. These re1262

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cordings were made off the Eastern Antarctic coastline near two Australian Antarctic stations. Eight recordings 共three from the same location兲 were made near Casey during 21 October–30 November and seven recordings 共each at a different location兲 were made near Davis during 8 November–1 December, for a total of 15 recordings made at 12 locations. The recordings were made during a period of 24 h light, near groups of females with pups on the ice. The number, sex and age of the vocalizing seals could not be determined, nor was it possible to determine the proximity of the seals to the hydrophone. Each recording lasted 1–2 h. At each recording site, one hole was drilled through the sea-ice and the hydrophone was lowered approximately 2 m below the ice. Sony TCD-D3 DAT recorders 共frequency response 0.02–20 kHz ⫾1 dB) were used to make the recordings. At Casey, an ITC 6050C hydrophone 共frequency response 0.002–30 kHz ⫾1 dB), with a built in preamplifier was connected to the Sony DAT recorder. At Davis, a Bru¨el and Kjær 8100 hydrophone equipped with a Bru¨el and Kjær 2635 charge preamplifier 共frequency response 0.002–30 kHz ⫾1 dB) was used.

B. Data analysis

Gram 共Version 6.0.9兲 was used to analyze the calls. A preliminary examination determined that six call type categories were the most commonly occurring multiple element call types on the recordings. These were Chugs 共C兲, Knocks 共K兲, Grunts 共G兲, Whistle-Ascending 共WA兲, WhistleAscending-Grunts 共WAG兲 and Whistle-Descending 共WD兲 calls 共Thomas and Kuechle, 1982; Thomas et al., 1988; Pahl et al., 1997兲. Only calls of these types were analyzed. The call type categories were highly variable and so were further classified into subtypes that described the calls in greater detail and allowed calls most similar to each other to be grouped together. Call types were separated into distinct subtypes based on relative differences in waveform, spectral shape, timing and frequency of the calls within any one call type. It is important to note that the criteria used to classify the calls into subtypes in this study were arbitrary, and the classification scheme was based on differences that were distinct to the observer. The subtypes chosen were based on small sample sizes and the calls were not necessarily sorted into subtypes based on the same classification scheme as reported by other authors 共Thomas and Kuechle, 1982; Thomas et al., 1988; Pahl et al., 1997; Abgrall et al., 2003兲. To restrict the possibility of analyzing a large number of calls from a single seal, an upper limit of 20 samples from each call type category 共with the exception of the highly variable WD calls兲 were analyzed from any one recording. Up to 40 WD calls were analyzed from a recording; however these calls included several WD subtypes. Many of the WD calls also overlapped each other in time 共though not usually in frequency兲. Therefore it is highly unlikely that any one seal made all of the WD calls at a single site. Only clear calls from which accurate measurements could be made repeatedly were chosen for analysis. For each multiple element call type examined, the following features were noted: H. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

共1兲共2兲共3兲共4兲

Call type category and subtype. Total number of elements in the call. Total length of the call. Element duration 共ms兲 of each element in the call, up to the first 30 elements of the call. Measures from only the first 30 elements of the call were made due to practical reasons 共time limitations兲, and because the majority of the calls analyzed 共84%兲 were less than 30 elements long. For the calls analyzed, the signal to noise ratios were high enough (⬎5 dB) to permit consistent measures of element length. 共5兲 Interval 共inter-element兲 duration 共ms兲 of each interval in the call, up to the first 29 intervals of the call. 共6兲 Frequency 共Hz兲 of elements in the call. The start and end frequencies (⫾43 Hz) of each element in a call were measured. Frequency measures were made at the midpoint of broad bandwidth calls.

Data obtained for the element and interval durations and frequency were transformed into proportional data. Each value of a measurement 共element or interval duration, or frequency兲 was transformed to a proportion of the previous measure. Transformed data for element durations was indicated as ‘‘proele,’’ for interval duration data as ‘‘proint,’’ and as ‘‘prost’’ or ‘‘proend’’ 共the start and end frequencies兲 for frequency data. Transformed data were used because some of the calls appeared to consistently increase or decrease in frequency and timing throughout the call. Such patterns would be expected to show a significant difference between means for the absolute 共raw兲 data. These same calls would be expected to show no or only slight difference between means for the transformed data if the increase or decrease in timing and frequency were regular 共a constant proportion of the previous measure兲. Both the absolute and transformed data were examined to determine consistency within the calls. For the absolute and transformed data the mean, standard deviation 共SD兲, and coefficient of variance 共CV兲 values were calculated for the element and interval durations of all calls. These basic statistics were also calculated for groups of calls of a particular number of elements 共NOE; 3–5, 6 –10, 11–20, 21–30, and ⬎30 elements兲, from a particular site 共Casey or Davis兲, or occurring with an apparent rhythm pattern. Using both absolute and transformed data, ANOVA’s were used to determine the consistency of element and interval durations within calls. The consistency of element and interval durations was also tested for calls with a specified NOE, from a particular site, or occurring with a particular rhythm pattern. Calls were then analyzed according to call type category and subtype. Mean, SD, and CV values of the absolute and transformed data for element durations, interval durations, and start and end frequencies of each element 关 log2(Hz) 兴 , were calculated for calls of each type and subtype. These values were also calculated for calls with a specified NOE, from a particular site, or occurring with a particular rhythm pattern within each type or subtype. ANOVA tests were then used to determine the similarity of measurements within each call type category and subtype. The total duration of the calls was also examined. The J. Acoust. Soc. Am., Vol. 116, No. 2, August 2004

mean total duration and SD values of calls consisting of a specific NOE were calculated. ANOVA’s were then used to compare mean call durations. III. RESULTS A. All calls—NOE, site and pattern effects

A total of 405 Weddell seal multiple element calls were examined. WD calls were the most common call type category, compromising 292 共72%兲 of the calls analyzed. Up to 40 WD calls were analyzed from 3 of the 15 recordings. These three recordings were made at one location near Casey. There was a high incidence of WD calls on these recordings, however fewer than 20 WD calls were analyzed from each of the other 12 recordings due to lower calling rates and fewer calls overall on the tapes. For most call type categories, the calls analyzed from each tape were separated in time along the recording because many were uncommon or had low signal to noise ratios, which prohibited obtaining accurate measurements. When all calls were examined together, the mean element durations 共mean duration of Element 1, mean duration of Element 2, mean duration of Element 3, etc.兲 were not significantly different from each other (F 29,6667⫽1.12,p ⫽0.299). Mean interval durations were significantly different from each other (F 28,6262⫽7.61,p⬍0.0001), due to large durations of the first few intervals. When the transformed data for interval durations were analyzed 共interval duration as a proportion of the previous interval duration兲, the mean interval durations were no longer significantly different (F 27,5857⫽0.79,p⫽0.770). When all calls were analyzed together, the SD and CV values for element and interval durations were large. Mean element durations had an average CV value of 1.19⫾0.36, and mean interval durations had an average CV value of 1.60⫾0.29. The SD values of the transformed data were smaller than those for the absolute data with the average CV value for the proele data being 0.38 ⫾0.11, and the average CV value for proint data being 0.52⫾0.41. 1. Trends related to the number of elements in a call

When calls were analyzed by NOE, calls with fewer elements tended to have longer element and interval durations than did calls with many elements 共Figs. 1, 2兲. Calls with many elements also appeared to be more stable, with fewer fluctuations in mean duration values 共Fig. 1兲. There was a tendency for longer calls with many elements to have slightly increasing element and interval durations throughout the calls 共Fig. 1兲. ANOVA results indicated significant differences in element and interval durations of calls with 21–30 elements 共elements: F 29,1966⫽4.22,p⬍0.0001, intervals: F 28,1889⫽14.90,p⬍0.0001), or ⬎30 elements 共elements: F 29,1949⫽4.86,p⬍0.0001, intervals: F 28,1884⫽9.94,p ⬍0.0001) due to increasing mean duration values. When analyzing calls by NOE, for all but two of the cases in which significant differences were found in element and interval durations, the mean durations of the transformed data were not significantly different 共all p-values ⬎0.102). For the cases in which the transformed data showed significant differences 共proele values of calls with 11–20 elements and H. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

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to be a high degree of variance near the beginning and end of the calls and when first and last few values were excluded from the tests, the mean durations were no longer significantly different. SD and CV values remained high for both element and interval durations, even when calls were analyzed by NOE. For example, the average CV value of calls 3–5 elements long was 0.87⫾0.11 共element durations兲 and 0.98⫾0.16 共interval durations兲. For the transformed data, the SD values were reduced and the average CV values were 0.25⫾0.08 共proele兲 and 0.23⫾0.05 共proint兲. 2. Differences in calls analyzed at each site

FIG. 1. Trends in mean duration values 共ms兲 of intervals 共I兲 and elements 共II兲 of Weddell seal multiple element underwater calls, analyzed by a specific number of elements 共NOE兲 per call: 3–5 elements 共⽧兲, 6 –10 elements 共•兲, 11–20 elements 共䉱兲, 21–30 elements 共䊏兲, and 30⫹ elements 共*兲. See text for details on variance associated with analyzing calls by NOE.

proint values of calls with 21–30 elements兲, there appeared

Of the 405 multiple element calls analyzed, 290 were recorded at Casey and 115 were recorded at Davis. Mean element durations showed no significant differences at either site 共Casey: F 29,5073⫽1.05, p⫽0.392, Davis: F 29,1593⫽1.01, p⫽0.451). Significant differences were found when analyzing mean interval durations 共Casey: F 28,4783⫽8.06, p ⬍0.0001, Davis: F 28,1478⫽3.38, p⬍0.0001). For both sites, when transformed data for interval duration were analyzed, means were not significantly different 共Casey: F 27,4493 ⫽0.51, p⫽0.983, Davis: F 27,1363⫽1.03, p⫽0.422). The average CV values for element durations for calls analyzed by site were 1.23⫾0.50 共Casey兲, and 0.80⫾0.10 共Davis兲. The average CV values for interval durations were 0.62⫾0.33 共Casey兲 and 1.07⫾0.34 共Davis兲. When the transformed data were considered, the SD and CV values were greatly reduced, with average CV values of 0.34⫾0.11 and 0.50 ⫾0.47 共Casey兲 and of 0.44⫾0.20 and 0.46⫾0.30 共Davis兲 for element and interval durations, respectively. Differences between sites may be attributed to differences in sample size of each of the call types and subtypes at each site 共Table I兲. 3. Rhythm patterns in Weddell seal calls

FIG. 2. Examples of timing patterns in Weddell seal multiple element underwater calls; I⫽Pattern cC 共subtype WD10 call displayed兲, II⫽Pattern iI 共subtype WD1 call displayed兲, III⫽Pattern cD 共subtype WD8 call displayed兲; see the text for an explanation of terms. Analyzing bandwidth ⫽86 Hz. 1264


Timing of the element durations 共indicated in lowercase letters兲, as well as the interval durations 共indicated in capital letters兲, were considered when categorizing calls into rhythm patterns. Patterns of duration timing were either constant 共indicated by the letters ‘‘c’’ or ‘‘C’’兲, increasing 共‘‘i’’ or ‘‘I’’兲 or decreasing 共‘‘d’’ or ‘‘D’’兲. Therefore, Pattern cI calls had constant element durations 共indicated by ‘‘c’’兲 and increasing interval durations 共indicated by ‘‘I’’兲 throughout the call. Seven rhythm patterns with respect to the timing of elements and intervals of the calls were identified in the Weddell seal vocalizations 共Patterns cC, iC, cI, iI, dI, cD, and iD; Table II; Figs. 2, 3兲. The most common rhythm for element durations was constant timing, while increasing interval durations was the most common rhythm for the interval timing. Decreasing timing was the most uncommon rhythm pattern for both element and interval durations 共Table I兲. The most common rhythms were Pattern iI and Pattern cC. Patterns cI and cD were also frequently emitted, while only a small fraction of calls were produced with the remaining three rhythm patterns 共Table I兲. None of the multiple element calls examined occurred without some form of patterning of the element and interval durations. H. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

TABLE I. The number of Weddell seal multiple element underwater calls of each of the seven patterns occurring within each of the call subtypes 共see the text兲. Patterns of duration timing were either constant 共indicated by ‘‘c’’ or ‘‘C’’兲, increasing 共‘‘i’’ or ‘‘I’’兲 or decreasing 共‘‘d’’ or ‘‘D’’兲. Whether a particular pattern occurs within the call subtype at just Casey 共Cas兲, at just Davis 共Dav兲, or at both sites 共Both兲 is indicated 共in brackets兲. The total sample size for each call pattern is also given 共Total兲. Pattern

Call Subtype WD1 WD2 WD3 WD4 WD5 WD6 WD7 WD8 WD9 WD10 G1 G2 G3 G4 C1 C2 C3 K1 K2 K3 WAG WA1 WA2 WA3 Total

cC

iC

cI

iI

dI

cD

2 共Both兲

3 共Cas兲

23 共Both兲 1 共Cas兲 3 共Dav兲 9 共Dav兲

97 共Cas兲 27 共Cas兲

5 共Cas兲

1 共Cas兲

8 共Cas兲

2 共Cas兲

3 共Cas兲 13 共Cas兲 26 共Dav兲 6 共Both兲 1 共Dav兲 2 共Dav兲 18 共Both兲 8 共Both兲 4 共Both兲

2 共Cas兲 1 共Dav兲

10 共Cas兲 8 共Dav兲 2 共Dav兲

1 共Dav兲 108

6

76

TABLE II. Average values of the mean element and interval durations 共standard deviation indicated in brackets兲 calculated for the transformed data 共duration as a proportion of the previous measure兲 for each of the seven timing patterns of Weddell seal multiple element underwater calls. Timing of the element durations 共ProEle; indicated by the lowercase letters兲, and interval durations 共ProInt; indicated by uppercase letters兲 were both considered when categorizing calls into patterns. Average duration value N

cC iC cI iI dI cD iD

108 6 76 140 5 54 16

2 共Dav兲

11 共Dav兲 1 共Cas兲 2 共Dav兲

4 共Dav兲

3 共Cas兲 5 共Cas兲 8 共Dav兲 3 共Dav兲

Pattern

24 共Both兲 27 共Cas兲

10 共Dav兲 5 共Cas兲 1 共Dav兲

The rhythm patterns of the calls became evident by listening to the calls and by analyzing the absolute and transformed data. With constant duration patterns the mean element or interval durations 共of the transformed data兲 tended to be close to 1.0 共Table II兲. This indicates that adjacent durations were approximately equal. When calls with increasing duration patterns were analyzed, mean durations tended to be greater than 1.0, usually above 1.1 共Table II兲 showing that durations were increasing as the calls progressed. This

a

13 共Cas兲

iD

ProEle 1.04 1.09 1.08 1.12 0.99 1.03 1.13

共0.042兲共0.124兲共0.124兲共0.091兲共0.106兲共0.142兲共0.268兲

ProInt 1.09 共0.204兲 1.05 共0.215兲 1.18 共0.090兲 1.19 共0.154兲 1.10 共0.182兲 0.99 共0.103兲a 0.99 共0.166兲a

The first interval durations are not included in calculations due to the fluctuation of values at the beginning of the calls. When the first two interval durations were included the mean duration in both cases 共for cD and iD calls兲 became 1.02 due to the presence of very high interval values within the first two intervals 共see the text兲.


140

5

54

16

rhythm was easily identified when listening to the calls or looking at spectrograms. When decreasing patterns were analyzed, the transformed data produced mean durations of slightly less than 1.0 indicating that durations were decreasing. Decreasing rhythm was not easily identified by just listening to the vocalizations, but became apparent on spectrograms and by examining the time data. For example, the averages of all the mean proint values for calls with Pattern cD or iD timing were actually slightly greater than 1.0 because these calls tended to have longer interval durations near the beginning of the calls before the interval pattern of decreasing timing became established. When the mean durations of the first two interval values were excluded, the values for the Pattern cD and iD calls dropped below 1.0 共Table II兲. Patterns of both element and interval durations tended to show fluctuations, particularly at the beginning and end of calls 共Fig. 3兲, however, the interval durations clearly demonstrated the constant, increasing or decreasing rhythm patterns, while the element rhythm patterns were not as evident. For the majority of cases when the absolute mean durations of elements and intervals were analyzed for the different rhythms, call attributes with constant timing showed no significant differences in mean duration values, while calls with increasing or decreasing timing did show significant differences 共due to apparent increasing or decreasing mean durations兲. There were some exceptions to this. In the case of the Pattern cC calls, both element and interval durations showed significant differences between means 共elements: F 29,1556⫽5.23, p⬍0.0001, intervals: F 28,1448⫽6.18, p H. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

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FIG. 3. Trends in mean element and interval durations of Weddell seal multiple element underwater calls occurring with each timing pattern: I⫽calls with constant interval durations 共Patterns cC, iC兲, II⫽calls with increasing interval durations 共Patterns cI, iI, dI兲, III ⫽calls with decreasing interval durations 共Patterns cD, iD兲. See the text for details on variance in calls analyzed by a rhythm pattern.

⬍0.0001). The initial element and interval durations were much longer than the remaining durations 共which may be attributed to the trend of shorter calls having longer element and interval durations兲. This may also account for the significant difference observed among mean element durations of Pattern cD calls (F 29,434⫽4.50,p⬍0.0001). Of the 14 ANOVA tests performed using the transformed data for calls of each rhythm; the values were not found to be significantly different from each other in 12 cases (11 p-values ⬎0.092;1 p-value⫽0.054). The two cases where significant differences were found were for proint values of Pattern cC calls and proele values of Pattern iI calls. The proele values for Pattern iI calls showed significant differences due to variation near the beginning of the calls. When all but the first few values were included in the test, the means were not significantly different. For the Pattern cC calls, one of the mean proint values was larger than the rest due to a long interval duration measured from a single call. When this outlier value was excluded from the analysis, the mean proint values were no longer significantly different. The SD and CV values of calls analyzed by pattern were smaller than when all calls were analyzed together. For example, the average CV values for element and interval durations of Pattern cC 共absolute data兲 were 0.81⫾0.29 and 1266


1.10⫾0.49, respectively. The average CV values for the transformed data were reduced to 0.29⫾0.16 共proele兲, and 0.49⫾0.43 共proint兲. B. Call type categories and subtypes

The calls classified under the six broad call type categories were arbitrarily separated into 24 subtypes. While there was only one type of WAG call, the rest of the call types were classified into several subtypes. The WD calls showed the highest amount of variability and were classified into 10 different subtypes 共Table I兲. The calls of any one subtype were most commonly emitted with only one or two rhythm patterns 共Table I兲. In the case of the WD1 calls, however, the calls occurred in six different timing patterns 共although 92% of the WD1 calls occurred as Pattern cI or iI calls; Table I兲. In some cases, call subtypes were found to occur at both sites but with different rhythm patterns at each site. Many call subtypes also occurred with the same rhythm, while other rhythms were specific to only a few subtypes 共Table I兲. Some subtypes demonstrating a specific rhythm had low sample sizes 共Table I兲. When calls were analyzed by call type category, SD and CV values of mean element and interval durations were genH. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

TABLE III. The mean, standard deviation 共in brackets兲 and coefficient of variance 共CV兲 of the frequencies 关 log2(Hz) 兴 measured at the beginning 共Start Frequency兲 and end 共End Frequency兲 of each element of all subtype WD1 Weddell seal multiple element underwater calls analyzed together. The number of the element from which the measures were taken is given 共Element Number兲, as well as the number of calls analyzed 共N兲. Start frequency Element #

N

1 2 3 4 5 10 15 20 25 30

131 131 131 130 130 119 86 54 36 19

Mean 12.96 12.83 12.76 12.73 12.68 12.55 12.29 12.06 11.60 11.53

共0.789兲共0.798兲共0.746兲共0.721兲共0.728兲共0.754兲共0.865兲共0.884兲共0.872兲共1.031兲

erally smaller than when all calls were analyzed together, or when all calls were analyzed by site or NOE. The average CV values for the element and interval durations of WD calls, the most variable call type, were 1.05⫾0.34 共element durations兲 and 1.45⫾0.37 共interval durations兲. The average CV values for the transformed data of the WD calls were 0.36⫾0.11 共proele兲 and 0.48⫾0.42 共proint兲. The SD and CV values obtained for calls analyzed by subtype were smaller than those of calls analyzed by call type categories. For example, the average CV values for WD1 calls were 0.89 ⫾0.35 共element durations兲 and 1.27⫾0.43 共interval durations兲. For the transformed data, average CV values were reduced to 0.33⫾0.13 共proele durations兲 and 0.39⫾0.22 共proint durations兲. When analyzing call type categories or subtypes from a particular site, having a specific NOE or occurring with a particular rhythm, SD and CV values were further reduced. The frequency 共kHz兲 of each call subtype was very consistent and had low SD and CV values 共Table III兲. Frequency of the calls followed three patterns: rising start frequencies throughout the calls 共displayed by subtypes G1 and WD3兲, falling start frequencies throughout the calls 共subtypes C1, WD1, WD2, WD5, and WD8兲 or constant frequencies 共subtypes C2, C3, G2, G3, G4, WD4, WD6, WD7, WD9, WD10, and all K, WAG and WA calls兲. For the majority of calls, the frequency tended to drop within individual elements; therefore start frequencies were typically higher than end frequencies 共with the exception of the WA calls兲.

End frequency CV

Mean

CV

0.06 0.06 0.06 0.06 0.06 0.06 0.07 0.07 0.08 0.09

12.09 共1.040兲 11.86 共0.901兲 11.60 共0.885兲 11.42 共0.876兲 11.19 共0.911兲 10.59 共0.950兲 9.83 共1.085兲 9.33 共1.122兲 9.29 共1.219兲 9.15 共0.911兲

0.09 0.08 0.08 0.08 0.08 0.09 0.11 0.12 0.13 0.10

IV. DISCUSSION A. Patterns in Weddell seal multiple element underwater calls

Element and interval durations were found to either increase, decrease or remain constant throughout any one call. In total, seven patterns of timing were identified. Both element and interval durations were used to determine the rhythm patterns within calls, however, interval rhythms were easier to identify than element rhythms 共Table II; Fig. 3兲. The stability of the patterns was demonstrated by examining the transformed data for calls occurring with each rhythm. For the majority of cases within the seven patterns, the mean durations of the transformed data were not significantly different from each other, indicating that the increasing, decreasing or constant element and interval durations were regular. The variation in mean values of element and interval durations 共absolute data兲 was high for calls of each rhythm. The variance may have been caused by differences between call type categories emitted with each rhythm, as most of the rhythm patterns were observed in several call types 共Table I兲. When patterns within each call type category or call subtype were analyzed separately, SD and CV values were reduced for absolute and transformed data. Variance may also be attributed to differences between individual seals. The beginning and ending elements and intervals of a call were the

C. Trends in total call length

The total length of the calls averaged 22⫾16.6 s. When the total lengths of the calls were analyzed by NOE, the mean total duration values ranged from 20 to 27 s. The SD values obtained for these means were high, however, the means were not significantly different from one another (F 4,404⫽1.83; p⫽0.122; Fig. 4兲. The calls with 31⫹ elements had the longest mean total duration 共Fig. 4兲. These calls included calls ⬎100 elements in length and therefore a greater mean duration value would be expected. However, the longest call 共114.4 s兲 was a 4-element call, while the shortest call 共1.9 s兲 was a 31-element call. J. Acoust. Soc. Am., Vol. 116, No. 2, August 2004

FIG. 4. Mean total length ⫾1 SD of Weddell seal underwater multiple element calls analyzed in groups according to the number of elements present in the call. H. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

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most variable. The rhythm often became more clearly established after the first few elements were emitted and persisted throughout the main body of the call. There were also stable frequency patterns found within the calls. The start frequencies of elements throughout any one multiple element call may either remain constant throughout the entire call, increase as the call progresses, or decrease as the call progresses. The subtypes of the calls were determined mainly by the spectrum shape of the calls, therefore the frequencies were very consistent for call subtypes regardless of pattern in which the calls were emitted 共Table III兲. The mean total duration of the calls analyzed 共22 s兲 did not vary with an increasing number of elements 共Fig. 4兲. This can be attributed to the fact that the element and interval durations tended to decrease as the number of elements within a call increased 共Fig. 1兲. Terhune et al. 共1994兲 suggested that when multiple element calls were overlapped, Weddell seals lengthen the duration of their calls by adding elements to the end of calls. The additional elements likely enhance detection of the calls by distant conspecifics. Contradictorily, the results of this study indicate that the seals do not just add elements to a call after the call has already begun, but predetermine the length of their calls prior to calling. A possible explanation is that the seals assess the level of background noise before calling and then plan their call with a predetermined NOE accordingly in order to maximize call detectability. Emitting calls with many elements would be the most beneficial during periods of high level background noise. This could be an example of an antimasking strategy used by the seals. The relatively stable total duration of the calls may also be due to a physiological restriction on the seals such as limits imposed by the physical size of their air chambers. However, multiple element calls of 65.3 s or 540 elements have been recorded in Weddell seals 共B. Pahl, unpublished data兲. The total number of seals that produced the 405 calls analyzed is unknown. The Weddell seal recordings analyzed included many calls overlapping in time 共but not in frequency兲, therefore it is likely that the calls were recorded from a number of seals at each site. It is possible that uncommon call subtypes were made by a single seal. The results in this study are biased towards loud source level calls, presumably from nearby seals that were not masked by other calls or noises. The call subtypes were determined subjectively, however, the broader call type classification system followed that reported in previous studies 共Thomas et al., 1988; Pahl et al., 1997兲.

B. Anti-masking properties of patterned calls

Acoustic communication requires not only detection, but also recognition of signals by a receiver 共Klump, 1996兲. Wiley and Richards 共1978兲 described two common tactics used by animals to combat degradation and masking of signals during transmission, and enhance the recognition of calls; 共1兲 coding and 共2兲 redundancy of information 共in this case, repetition of call elements兲. Patterning and repetition of 1268


signals helps the receiver to differentiate between signals and noise 共Bateson, 1968兲, and ensures accurate transmission of signals 共Wiley and Richards, 1978兲. The presence of rhythmical repetition in seal communications has important implications for the extent to which seals can successfully communicate over long distances and during high levels of background noise. Having stereotyped rhythmic patterns in their underwater vocalizations likely confers a number of advantages that would facilitate Weddell seal communication. In quiet surroundings, the repetition of the call elements likely enhances their detection relative to a single element call. This could potentially increase the detection range of a call by up to 80% 共Turnbull and Terhune 1993兲. Most ice noises occur as single events and the regular repetition would distinguish multiple element calls from abiotic sources 共Watkins and Schevill, 1979兲. When other seals are calling or the abiotic noise levels are high, the calls are more likely to be detected when the elements are repeated in a regular manner. Such calls will be longer and thus it is less likely that the entire call would be completely masked by other sounds. Once the first few elements of the multiple element call are emitted 共thereby establishing the call pattern兲, listening conspecifics would theoretically be able to predict when successive elements should occur. If a listener was uncertain about the presence of a faint call, the regular repetition would enable them to confirm its presence by knowing when to expect subsequent elements. Chickadee 共Poecili carolinensis兲 calls were found to contain a form of repetition, where properties of single notes provided cues about the syntactical structure of the entire call. A listener would only have to detect a portion of the call in order to receive the entire message 共Freeburg et al., 2003兲. By increasing call length through the addition of elements 共Serrano and Terhune 2001兲, and by producing these elements at regular intervals, Weddell seals may be able to enhance the probability of call detection by a listener. Similarly, king penguins increase the number of elements in their calls when increasing wind speeds raise the level of background noise. By increasing the repetition of information during times of high levels of background noise, the birds could increase the probability of communicating during short time windows when the noise level drops 共Lengagne et al., 1999兲. C. Possible functions of call patterning

Various animal species use patterns in timing of call elements in order to recognize signals produced by conspecifics. Grasshopper and cricket stridulations, and flash patterns produced by fireflies are often species specific 共Alexander, 1968; Helverson and Helverson, 1998; Ronacher et al., 2000兲. Studies of tree-frog mating calls have shown that timing structure of the calls encodes information about the species and sex of the frog making the calls 共Schwartz et al., 2002; Wollerman and Wiley, 2002兲. Bird songs may be unique to a species or an individual. Studies of rhythm in bird vocalizations have shown characteristic patterns emerging in songs of different bird species, regardless of whether the songs were developed through independent learning of an individual or through interactions of the individual with other birds. Rhythms present in songs of different species of H. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

doves, pigeons, sparrows and shore birds have been statistically demonstrated 共Baptista, 1996; Miller, 1996兲. Generally, variation in the duration of individual notes 共elements兲 and the intervals between the notes in complex vocalizations are found to provide rhythms characteristic of a species 共Baptista, 1996兲. Within the distinctive calls of the Carolina chickadee, the ordering of the elements within the call were not only species specific, but single elements within the calls were predictive of the bird’s local capture site as well 共Freeburg et al., 2003兲. It is also possible that the patterns with which Weddell seals emit calls may serve species or individual recognition functions. Improved species detection should occur if the receiver has only a few patterns to listen for. The seven rhythm patterns used by Weddell seals 共which consist of only three timing trends; constant, increasing and decreasing兲 do not likely match those of other seal species in the area. The groan-like call of crabeater seals 共Lobodon carcinophagus兲 is a low frequency, single-element long duration call 共Stirling and Siniff, 1979兲. Leopard seals 共Hydrurga leptonyx兲 typically produce single or double-element calls, the majority of which are trills that have frequency and duration patterns very different from Weddell seals 共Stirling and Siniff, 1979; Rogers et al., 1995; Thomas and Golladay, 1995兲. Ross seals 共Ommatophoca rossi兲 produce pulsed sounds interspaced with long frequency modulated tones. Spectrograms of these calls showed different patterning than that of calls produced by Weddell seals 共Watkins and Ray, 1985兲. Sperm whales studied in the Mediterranean Sea produced click sequences consisting of four clicks 共elements兲. The durations of these elements were found to be highly variable, while inter-click 共interval兲 durations occurred in a 2:1:1 rhythmic pattern. It was suggested that the timing of the highly stable intervals, rather than the variable-length clicks of click sequences contained the information in the calls 共Pavan et al., 2000兲. It was also found that the patterning within harp seal calls occurred in the interval rather than the element timing 共Moors and Terhune, 2003兲. Unlike the sperm whale and harp seal calls, both the element and interval durations of the Weddell seal calls occurred in specific patterns. This suggests that both the elements and the intervals of the call may contain information. It is important to note, however, that the patterns of interval duration in the calls are more stable and easier to identify than the element timing patterns 共Table II; Fig. 3兲. The call patterns identified in harp and Weddell seals are similar in many ways but they do exhibit fundamental differences. While the timing and frequency within harp seal multiple element call patterns is constant, the Weddell seal calls display timing and frequency shifts throughout the calls. Weddell seal element and interval durations also tend to be influenced by the number of elements within the call. This did not occur in the harp seal calls 共Moors and Terhune, 2003兲. For the Weddell seal calls, the waveform, bandwidth, and frequency range of individual call types exhibit considerable variation 共Thomas and Kuechle, 1982; Pahl et al. 1997兲. If the species recognition for Weddell seals resides in the temporal patterns of the multiple element calls, perhaps J. Acoust. Soc. Am., Vol. 116, No. 2, August 2004

the fine structure of the vocalizations is less important. Sounds given using the patterns would be distinct from random background noise and would match the familiar temporal model. Thus, the patterns of Weddell seal calls could serve to identify the species of the caller, independent of the frequency or waveform of the specific call type. Rhythms within Weddell seal calls may also potentially encode information on the behavior or situation of the calling seal. The barking rate of an adult male California sea lion 共Zalophus californianus兲 increased from 2.1 to 3.0 barks/s in air and from 1.0 to 1.4 barks/s underwater when the social context changed from nondirectional self advertisement, to chasing or confronting another sea lion 共Schusterman, 1977兲. Diana monkeys 共Ceriopithecus diana diana兲 emit long distance vocalizations which indicate the presence of very specific predators to conspecifics. These warning calls consist of a discrete number of syllables that varies depending on the type of predator present. Zuberbuhler et al. 共1997兲 found a significant difference for the overall call length and the intersyllable 共interval兲 durations between Diana monkey calls produced in the presence of leopards 共Panthera pardus兲 and those produced in the presence of hawk eagles 共Stephanoaetus coronatus兲. In the case of Weddell seal vocalizations, some of the variation within call rhythm patterns 共for example, differences in rhythm between call types兲 may be related to the calls being emitted in different behavioral contexts. Before this can be determined the behavior of individual vocalizing seals has to be studied at the call rhythm level. The consistency of timing within Weddell seal calls is demonstrated by the mean element and interval durations, which were relatively stable between each of the call subtypes 共within the seven patterns兲 as well as within the patterns themselves. There was some variance in element and interval durations of the calls, although this may be due to the use of very precise time measures. The ability of seals to detect a difference of a few milliseconds is likely limited, although studies on this topic have not been conducted. There is some variation within the patterns, but the patterns themselves are very distinct, and thus listeners would be expected to have little confusion when trying to identify a specific call rhythm. Further studies of seal call predictability are required in order to determine the extent to which rhythmically repeated calls aid in seal communication, if patterns emitted by seals serve a function for species identification, or if they carry information about the behavioral context in which the call is being made. The direct observation of individual calling seals will be required to determine the functional significance of the different vocalizations. ACKNOWLEDGMENTS

We thank H. Burton of the Australian Antarctic Division and the Australian National Antarctic Research Expeditions 共ANARE兲 for logistical support at Davis and Casey. D. Simon provided the recordings from Casey. H. Hunt, S. Turnbull and P. Rouget provided advice on an earlier draft of this manuscript. The National Science and Engineering ReH. B. Moors and J. M. Terhune: Repetition in Weddell seal calls

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search Council of Canada 共NSERC兲 provided funding for this project with a USRA to H. B. M. and Discovery Grant to J. M. T. Abgrall, P. A., Terhune, J. M., and Burton, H. R. 共2003兲. ‘‘Variation of Weddell seal 共Leptonychotes weddellii兲 underwater vocalizations over mesogeographic ranges,’’ Aquat. Mamm. 29, 268 –277. Alexander, R. D. 共1968兲. ‘‘Arthropods,’’ in Animal Communication: Techniques of Study and Results of Research, edited by A. Sebok 共Indiana University Press, London兲, pp. 167–217. Baptista, L. F. 共1996兲. ‘‘Nature and it’s nurturing in avian development,’’ in Ecology and Evolution of Acoustic Communication in Birds, edited by D. E. Kroodsma and E. H. Miller 共Cornell University Press, Ithaca兲 pp. 39– 60. Bateson, G. 共1968兲. ‘‘Redundancy and coding,’’ in Animal Communication: Techniques of Study and Results of Research, edited by A. Sebok 共Indiana University Press, London兲, pp. 167–217. Bertram, G. L. C. 共1940兲. ‘‘The biology of the Weddell and crabeater seals,’’ Scientific Reports, British Graham Land Expedition 1934-1937, 1, 1–139. Freeburg, T. M., Lucas, J. R., and Lucas, B. 共2003兲. ‘‘Variation in chickadee calls of the Carolina chickadee population, Poecile carolinensis: identity and redundancy within notes,’’ J. Acoust. Soc. Am. 113, 2127–2136. Green, K., and Burton, H. R. 共1988兲. ‘‘Annual and diurnal variations in underwater vocalizations of Weddell seals,’’ Polar Biol. 8, 161–164. Hawkins, A. D., and Myrberg, A. A. 共1983兲. ‘‘Hearing and communication underwater,’’ in Bioacoustics: A Comparative Approach, edited by B. Lewis 共Academic, New York兲, pp. 347– 405. Von Helverson, D., and Von Helverson, O. 共1998兲. ‘‘Acoustic pattern recognition in a grasshopper: processing in the time or frequency domain?’’ Biol. Cybern. 79, 467– 476. Klump, G. M. 共1996兲. ‘‘Communication in the noisy world,’’ in Ecology and Evolution of Acoustic Communication in Birds, edited by D. E. Kroodsma and E. H. Miller 共Cornell University Press, Ithaca兲, pp. 321–338. Kooyman, J. L. 共1981兲. Weddell Seal: Consummate Diver 共Cambridge University Press, New York兲. Lengagne, T., Aubin, T., Lauga, J., and Jouventin, P. 共1999兲. ‘‘How do king penguins 共Aptenodytes patagonicus兲 apply the mathematical theory of information to communicate in windy conditions?’’ Proc. R. Soc. London, Ser. B 266, 1623–1628. Miller, E. H. 共1996兲. ‘‘Acoustic differentiation and speciation in shorebirds,’’ in Ecology and Evolution of Acoustic Communication in Birds, edited by D. E. Kroodsma and E. H. Miller 共Cornell University Press, Ithaca兲, pp. 39– 60. Moors, H. B., and Terhune, J. M. 共2003兲. ‘‘Repetition patterns in harp seal 共Pagophilus groenlandicus兲 underwater multiple element calls,’’ Aquat. Mamm. 29, 278 –288. Oetelaar, M., Terhune, J. M., and Burton, H. R. 共2003兲. ‘‘Can the sex of a Weddell seal 共Leptonychotes weddellii兲 be identified by its surface call?,’’ Aquat. Mamm. 29, 261–267. Pahl, B. C., Terhune, J. M., and Burton, H. R. 共1997兲. ‘‘Repertoire and geographic variation in underwater vocalizations of Weddell seals 共Leptonychotes weddellii, Pinnipedia: Phocidae兲 at the Vestfold Hills, Antarctica,’’ Aust. J. Zool. 45, 171–187. Pavan, G., Hayward, T. J., Borasani, J. F., Priano, M., Fossati, C., and Gordon, J. 共2000兲. ‘‘Time patterns of sperm whale codas recorded in the Mediterranean Sea 1985–1996,’’ J. Acoust. Soc. Am. 107, 3487–3495. Pollack, G. 共2000兲. ‘‘Who, what, where? Recognition and localization of acoustic signals by insects,’’ Curr. Opin. Neurobiol. 10, 763–767. Ray, C. 共1967兲. ‘‘Social behavior and acoustics of the Weddell seal,’’ Antarctic Journal of the United States 2, 105–106. Richardson, W. J. 共1995兲. ‘‘Marine mammal hearing,’’ in Marine Mammals and Noise, edited by W. J. Richardson, C. R. Greene, C. I. Malme, and D. H. Thompson 共Academic, Boston兲, pp. 205–240. Rogers, T., Cato, D. H., and Bryden, M. M. 共1995兲. ‘‘Underwater vocal

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H. B. Moors and J. M. Terhune: Repetition in Weddell seal calls