Diving patterns of harbour seals (Phoca vitulina) in the Wadden Sea, the Netherlands and Germany, as indicated by VHF telemetry

Edith H. Ries, Ilona M. Traut, Petra Paffen, and Paul W. Goedhart

Abstract: The diving behaviour of 25 harbour seals, Phoc-cr vitulinu (14 females and 1 1 males), of various body lengths was monitored by means of VHF telemetry at different locations i n the Wadden Sea during late autumn in 1991 and 1992. Median dive durations for individual seals ranged from 46 s to 2.9 min. The maximum dive recorded was 3 1 min, performed by an adult male, which represents the longest dive reported for harbour seals. Dive endurance increased significantly in relation to body length. Feniale harbour seals tended to perform fewer short dives and had a more narrow distribution of dive times. We detected no diurnal differences in dive behaviour and only the ambient air temperature was found to influence the duration of surface periods, in that surface intervals tended to be shorter when temperatures were below 9°C. The overall mean percentage of dive time was 85%, with individuals varying from 76 to 93%, and was i n general higher in females.

RCsumC : Nous avons etudik le comportement de plongee chez 25 Phoques communs, Phocu vitulincr (14 femelles et 1 1 miles), de tailles diverses au moyen d'un systitnie de telCmCtrie VHF. i differents points dans la nier des Wadden, i la fin des automnes de 1991 et 1992. La duree mediane des plongees se situait entre 46 secondes et 2.9 n i i n . La duree maximale de plongee a Cte evaluCe i 31 min, chez un mile adulte, ce qui represente la plongee la plus longue jamais enregistree chez un Phoque commun. L'endurance augnientait significativenient avec la longueur du corps. Les femelles avaient tendance h effectuer des plongees plus courtes et moins frequentes et l'etendue des durees de leurs plongees etait plus restreinte. Le comportement de plongde ne variait pas au cours de la journee et le seul facteur qui affectait la duree des pkriodes passees en surface Ctait la temperature de l'air: les phoques passaient moins de temps en surface lorsque la temperature etait infkrieure h 9°C. Le pourcentage nioyen du temps passe en plongee etait de 85% (76-93%) et etait genkralement plus eleve chez les femelles. [Traduit par la Redaction]

Introduction diving with a variety of activities ranging from foraging,

Harbour seals (Phoca vijulina) are adapted to a variety of habitat types. Steep rocky shores as well as shallow sandy coasts sustain large populations along both coasts of the North Atlantic Ocean. Apart from occasional haulout bouts, seals spend most of the time in the water. As top predators, seals optimise their foraging strategy by spending a high proportion of the time submerged (Kooyman 1985; Fedak et al. 1988; Feldkamp et al. 1989; Goebel et al. 199 1 ; Boyd et al. 1995). Harbour seals usually forage in shallow bays and coastal zones but are also capable of diving down several hundred metres (Stewart and Yochem 1989; BjBrge et al. 1995), foraging opportunistically on various species of fish or cephalopods (Havinga 1933; Behrends 1985; Pierce et al. 199 1 ; Thompson et al. 199 1). At sea, the animals combine

Received February 28, 1997. Accepted June 12, 1997.

E.H. Ries' and P. Paffen. Department of Aquatic Ecology. Institute for Forestry and Nature Research., P.O. Box 167, 1790 AD Den Burg, the Netherlands. I.M. Traut. Department of Aquatic Ecology, University Oldenburg, P.O. Box 2503, 261 1 1 Oldenburg, Germany. P. W. Goedhart. Centre for Biometry Wageningen, P.O. Box 16, 6700 AC Wageningen, the Netherlands.

' Author to whom all correspondence should be addressed (e-mail: e.h.ries@ibn.dlo.nl).

travelling, and resting to social interactions. In the shallow, highly productive ecosystem formed by

the Wadden Sea, several species of tlatfish occur in high densities, constituting the predominant prey of the resident harbour seal population (Dankers and de Veen 1978; Behrends 1985; Sievers 1989). Here, the animals are able to forage near their haulout sites, where average water depths at high tide range from 1 to 3 m over the flats and from 5 to 20 m in the channels. Tidal amplitudes range between 1.4 and 3.8 m (Dijkema et al. 1989).

The harbour seal population in the Wadden Sea has been the sub-ject of numerous studies. Yet the accumulated knowl- edge on the biology and behaviour of this population is primarily based on data collected from animals at terrestrial haulout sites (Wipper 1974; Reijnders 1976; Drescher 1979), while little is known about diving and, particulal-ly, foraging behaviour.

In this study the diving behaviour of free-ranging harbour seals was monitored by means of VHF telemetry. We inves- tigated the dive patterns of 25 animals and we report on size- and sex-specific differences in dive parameters.

Material and methods

The study was conducted throughout the Dutch and German Wadden Sea during late autumn in 1991 and 1992. Seals (14 females, 1 I males)

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Fig. 1. Frequency distribution of dive times and surface intervals for each seal as a box-and-whisker diagram. The box spans the interquartile range (25% quantile to 75% quantile) of dive times and surface intervals, with a line indicating the median. Whiskers extend beyond the ends of a box as far as the minimum and maximum values. Note that the maximum dive time for seal 23. which was 1860 s, is not displayed (see Table I for the sequence of dive times and surface intervals). The maximum surface intervals for seals 17, 20, 24, and 25, which are 445, 22 1 , 322, and 665 s, respectively, are also not displayed.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Seal number

Seal

of different body lengths, ranging from 95 to 159 cm, were caught close to haulout sites by setting a long standing net from a speed- boat. Captured animals were physically immobilised for the tagging procedure. The sex of each individual was determined and the body length (straight length from the nose to the tip of the tail) measured to the nearest centimetre. Based on the body length, as determined by Norgaard and Larsen (199 1) and P.J.H. Rei,jnders (unpublished data) for harbour seals originating from the Danish and Dutch Wadden Sea, respectively, the numbers of individuals representing the three age-classes were as follows: 4 juveniles (up to I year), 12 subadults (1 -4 years), and 9 adults (older than 4 years).

A VHF radio transmitter operating on a unique frequency was attached to the fur on the seal's head using quick-setting epoxy (Fedak et al. 1983). The transmitters were programmed to emit different patterns of signals according to the behaviour of the animal. During dives, signal emission was interrupted by a salt- water switch. Upon surfacing, a series of 8 rapid pulses at intervals of 1 s were emitted, followed by a slower mode with I pulse every 2 s. The transmitters were designed to last up to 9 months and had a receiving range of approximately 10 - 15 km.

number

Data collection The tagged seals were tracked using n~ultichannel receivers (Yaesu FT 2900) in combination with a directional Yagi antenna from either a boat or a car. The location of the observer was chosen to optimise receiving quality. When weak signals or radio interference rendered identification of signals questionable, the data were re,jected.

The diving behaviour of seals was monitored using a stopwatch; we noted the time of the first signal emitted by the transmitter in the fast-pulse mode (interpreted as surfacing of the animal and, hence, the beginning of a surface interval) and the time of the last signal received (considered to represent the termination of the breathing bout, i.e., the beginning of the next diving period). We defined a dive as the time interval between the last radio signal received and the first signal of the fast-pulse mode emitted upon surfacing. Only complete dive cycles, comprising a dive and the subsequent surface interval, were used in the analysis.

Dive data from individual seals were collected in sessions rang- ing from 30 min to 4.5 h. We made every effort to monitor each seal on several occasions during the study period. covering different stages of the tide as well as different time periods throughout the

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Table 1. Sequence of dive times and surface intervals for seal 23, recorded between 14:OO and 18: 13 on 16 November 199 1.

Dive duration (s) Surface interval (s)

Mean 9.4

Mean % dive time 96.3

day and night. During each session, the weather conditions were noted, including air temperature, wind speed, sky cover, and pre- cipitation. For each location the local tide table was used to deter- mine the time period for high tide, defined as the time interval for water levels above the mean tidal level, and for low tide, defined as the time interval for water levels below the mean tidal level. We defined the day as the period from half an hour before sunrise to half an hour after sunset.

Data processing A formal statistical analysis of dive and surface times was per- formed in the following way. Dive times were first log-transformed, as one would expect multiplicative effects instead of additive effects. Moreover, a log transformation makes the distribution of the dive times more symmetric. For each seal - observation period combination, the distribution of dive times was summarised into 10, 25, 50, 75, and 90% quantiles. Each quantile was then n~odelled separately using restricted maximum likelihood (Searle et al. 1992) with a random model (seallperiod). This takes proper account of the dependence structure in the data, i.e., observations on different seals are considered to be independent but observations on the same seal are assumed to be dependent. The restricted maximum likeli- hood analysis was weighted using the number of observations on which a quantile was based as weights. Fixed effects, like sex, length, tide, and weather conditions, were selected by means of

Table 2. Regression coefficients for quantiles of log dive times for the model a, + P(length - 90), where i = 1.2 for female and male seals, respectively.

Quantile SE

( % a l ~ ~ ~ ~ ~ ~ ~ a n l d ~ ~ ( ~ 1 1 ~ 1 1 1 3 1 ~ - a,na~C) 6 SE (0)

backward selection using Wald tests. Surface times were analysed in the same way. The analyses were done using the statistical pack- age Genstat 5 (1993).

Results

For the 25 tagged seals, a total of 124.5 h of dive activity and 20.3 h of surface time is presented in this study. Individuals were followed for various numbers of observation periods, ranging from 2 to 13, depending on success in locating the seal and the lifetime of the transmitters. As not all seals were equally accessible for data collection, the sample sizes vary among seals. The number of complete cycles obtained for each seal ranged from 29 to 291 and the total observation time from 7 1 to 835 min. The percentage of dive time in the total observation time ranged from 76 to 93%, with a mean of 85%.

The recorded dive and surface times were highly variable, both within seals and across individuals. This is shown in Fig. 1 , which displays the distribution of the pooled dive and surface times for each seal in a separate box-and-whisker diagram. Note that the seals are sorted according to body length. The distribution of dive times is skewed to the higher values for most seals, among individuals the median dive duration varied between 46 and 174 s and the median of the surface times between 7 and 32 s. As indicated by the 75% point of the distribution, there is some increase in dive time with body length. The longest dive recorded was 31 min, performed by an adult male during a 4-h observation period, when the animal performed a series of prolonged dives. Table 1 shows the complete sequence of dive durations and subsequent surface intervals.

The formal statistical analysis of the quantiles of the log- transformed dive times revealed that sex and length were the only significant explanatory variables. The extreme dive times of seal 23, which were all observed in the same period, were left out of the statistical analysis. Corresponding sur- face times were not included, as these extreme dives seemed to be outside the "normal" behavioural pattern of seals. Sex is significant for both the 10% ( p = 0.038) and 25% ( p = 0.029) quantiles, while length is significant for the 75 % ( p = 0.022) and 90% ( p = 0.006) quantiles. For the 50% quantile, both length ( p = 0.031) and sex ( p = 0.057) are relevant. Regression coefficients of the model with sex and length are given in Table 2 and a graphical representation of the fitted models on the original scale in Fig. 2. These data show that female seals do not perform as many short dives

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Fig. 2. Relationship between the dive times (min) and body lengths of male ( a ) and female (b) seals split into quantiles of 10, 25, 50, 75, and 90%. Each quantile was modelled separately using a restricted maximum likelihood model.

(a) (b)

Length of seal (cm)

Fig. 3. Relationship between the surface intervals and body lengths of all seals, split into quantiles of 10, 25, 50, 75, and 90%. Each quantile was modelled separately using a restricted maximum likelihood model.

Length of seal (cn i )

as male seals, while there is no difference in the percentage of long dives, i.e., female seals have a narrower dive-time distribution than male seals. The effect of length indicates that the lower tail of the distribution is more or less invariant to length, while the upper tail is stretched for longer seals.

Length seal

Table 3. Regression coefficients for quantiles of log surface times for the model a + P(1ength - 90).

Quantile ( % I a P SE (0)

Statistical analysis of the quantiles of the log-transformed surface times showed that length is the only significant explanatory variable, but only so for the higher quantiles. The p values for the 50, 75, and 90% quantiles are 0.066, 0.020, and < 0.00 1 , respectively. Regression coefficients of the model with length only are given in Table 3 and a graphi- cal representation of the fitted models in Fig. 3. The effect of length indicates that the lower tail of the distribution is invariant to length, while the upper tail is stretched for longer seals. With respect to the other explanatory variables, it was found that temperature had a significant effect on the 10% ( p = 0.048), 25% ( p = 0.008), and 50% ( p = 0.004) quan- tiles. For temperatures of 10°C and higher, the 10, 25, and 50% quantiles were a factor of 1.38, 1.49, and 1.34 larger respectively, than for temperatures of 9°C and lower. This implies that shorter surface times were more frequent for lower temperatures.

On average, harbour seals spent 85% of the time sub- merged during dive cycles; individuals varied between 76 and 93 %. No relationship was found between the percentage of time spent submerged and any of the explanatory variables.

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Discussion

Among 25 harbour seals freely diving in the Wadden Sea, the durations of dives varied considerably, with a high propor- tion of dives lasting less than 2 min and a small proportion of exceptionally long dives. The maximum recorded dive time was 31 min, performed by an adult male, which repre- sents the longest dive reported in harbour seals. This is in line with the maximum diving duration in relation to body mass for phocid seals predicted by Schreer and Kovacs (1997). During the 4-h observation period, seal 23 continued to perform prolonged dives; the mean duration was 9.4 min, with comparatively short surface intervals. Prolonged dives in bouts that may last many hours, with no apparent increase in the time spent at the surface, which were also reported for southern elephant seals (Mirounga leoninu) by Hindell et al. (1992), generally constitute a very small proportion of recorded dive durations in seals (e.g., Kooyman 1989; Le Boeuf et al. 1989; DeLong and Stewart 199 1 ; Castellini et al. 1992; Thompson and Fedak 1993).

Median dive durations varied among individuals from 46 s to 2.9 min and were found to increase with body length. The observed increase in dive duration with size has also been described for Weddell seals (Leptonychotes weddelli) (Kooyman et al. 1983) and northern elephant seals (Miroungu ungustirostris) (DeLong and Stewart 199 l ) , and can be attributed to the scaling relationship of metabolic rates (Kleiber 1961) and the size-related increase in body oxygen stores in phocids (Kooyman 1985).

Especially in the four smallest seals, most dives lasted less than 2 min and longer dives were rarely recorded. In larger1 older animals the distribution of dive times was skewed towards longer dives. Possibly, as the four juvenile seals in our study were only 3-4 months old by the time they were tagged, the breath-hold capacity was not yet fully developed (Jones et al. 1973; Lydersen and Hammill 1993). A similar pattern of dive durations, i.e., a preponderance of shorter dives, was also observed in immature Weddell seals (Kooy- man et al. 1983).

Dives of subadult and adult seals in our study tended to be shorter than the average dive duration of 2.5 min for harbour seals observed around Orkney (Fedak et al. 1988; D. Thompson, personal communication) and Norway (BjBrge et al. 1995). This could be related to the substantial differ- ences in water depth among these habitats. While foraging in the Wadden Sea, harbour seals were repeatedly observed to dive along the edge of the tidal channels, usually in water no deeper than 5 - 10 m, whereas in the Norwegian study some of the animals were foraging and diving down to 200 m. A number of studies revealed that in seals, dive duration increases in relation to maximum depth of the dive (Croxall et al. 1985; Boyd and Arnbom 199 1 ; DeLong and Stewart 1991 ; Ponganis et al. 1992; Harcourt et al. 1995). In terms of foraging efficiency, shallow dives take up less travel time, permitting the animal to spend a higher proportion of time at depth hunting prey (Houston and Carbon 1992; 'Thompson et al. 1993). However, with the high prey density encoun- tered in the Wadden Sea, continuously searching for food and, hence, performing longer dives are not necessary (Dankers and de Veen 1978; Thompson et al . 199 1). The

comparatively high proportion of short dives and the occa- sionally recorded long surface intervals observed in the older seals could be related to activities other than foraging.

The small but significant differences in diving patterns between male and female harbour seals detected in this study, i.e., females performed fewer short dives and had, on average, a higher proportion of dive time, might be due to subtle differences in foraging strategies between the sexes. Ralls et al. ( 1995) reported. that juvenile male California sea otters had developed a distinct diving behaviour in going further offshore and diving in deeper water to forage than females. Unfortunately we were not always able to locate the animals during this study, but recent developments in the production of small time-depth recorders and satellite tags will provide the improvements in technique necessary to fur- ther investigate this aspect in future studies on the foraging ecology of harbour seals.

Dive durations in our study were found to be highly varia- ble, especially in older seals, sometimes even exceeding the calculated aerobic dive limit (Kooyman et al. 198 1 ; Le Boeuf et al. 1989). During such long dives, recorded also in grey seals (H~1icho~ru.s gypus), harbour seals, and Saimaa ringed seals (Phocu hispidu .suimensi.s), animals were occasional 1 y observed to rest, apparently asleep, in shallow water (Fedak et al. 1988; Thompson et al. 199 1 ; McConnell et al. 1992; Hyviirinen et al. 1995). Prolonged dives may be related to hypometabolisni, which may occur during sleep (Castellini et al. 1992; Reed 1992; Boyd and Croxall 1996).

The mean percentage of time spent submerged in the total observation time reported in our study, 85 %, is typical for most phocids and confirms that diving activity of the seals does not appear to be costly (e.g., Kooyman 1989; Thomp- son et a]. 1993). The animals in our study performed many short and some very long dives with a high percentage of dive time, which suggests that only a fraction of dives might be dedicated exclusively to foraging. This is consistent with the shallow depths and abundance of prey in the Wadden Sea.

Acknowledgements

The study was supported by the Commission of the European Communities (Contract No. NORSPA 92- 1 IINTIOO, BA-30301 921010091) and the Dutch Ministry of Agriculture, Nature Management and Fisheries. We are grateful to the staff of the patrol vessels MS Hcirder, MS Krukel, and MS Phocu for logistic support and help during the tagging program. This work relied upon the assistance of many colleagues and stu- dents who participated in the fieldwork. We are grateful to Jane Reed, Dave Thompson, and Mike Fedak for enlighten- ing discussions and valuable comments on the manuscript.

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