Behavioral and physiological reactions of arctic seals during under-ice pilotage

Behavioral and physiological reactions of arctic seals during under-ice pilotage1

ROBERT ELSNER Institute of Marine Science, University of Alaska Fairbanks, Fairbanks, AK 99775-1 080, U. S. A.

DOUGLAS WARTZOK Department of Biological Science, Purdue University, Fort Wayne, IN 46805-1 499, U. S. A.

AND

NANCY B. SONAFRANK AND BRENDAN P. KELLY Institute of Marine Science, University of Alaska Fairbanks, Fairbanks, AK 99 775-1 080, U. S. A.

Received November 25, 1988

ELSNER, R., WARTZOK, D., SONAFRANK, N. B., and KELLY, B. P. 1989. Behavioral and physiological reactions of arctic seals during under-ice pilotage. Can. J. Zool. 67: 2506 -25 13.

One spotted seal (Phoca largha) and two ringed seals (Phoca hispida) were studied in experiments designed to determine which sensory modalities were employed in pilotage from one under-ice breathing hole to another. Breathing holes were drilled in the ice of a frozen freshwater pond and a lake near Fairbanks, Alaska. Holes were located 22 - 150 m apart. Tethered seals swimming without blindfolding located holes when they chanced to swim within visual detection distance. Blindfolded seals responded to acoustic signals. Tactile sensitivity of the vibrissae was used by blindfolded seals in the immediate vicinity of a hole to which they had been attracted by an acoustic cue. Responses of a juvenile ringed seal did not differ fundamentally from those of an adult of the same species nor from those of the spotted seal. The results indicate that seals relied upon a sensory hierarchy for locating breathing holes: vision, audition, and vibrissal sense. Heart rate was recorded during voluntary dives of the younger ringed seal at 2 and 3 years of age. Profound diving bradycardia was observed, suggesting that a highly developed diving response is routinely invoked by seals of relatively small body size during under-ice excursions.

ELSNER, R., WARTZOK, D., SONAFRANK, N. B., et KELLY, B. P. 1989. Behavioral and physiological reactions of arctic seals during under-ice pilotage. Can. J. Zool. 67 : 2506-2513.

Des exgriences sur un Phoque commun (Phoca largha) et deux Phoques annelCs (Phoca hispida) ont permis de dkterminer quelles voies sensorielles sont utilisCes lors des dkplacements sous l'eau d'un trou de respiration B un autre. Des trous de respiration ont CtC forks dans la glace d'un Ctang d'eau douce gel6 et dans un lac, prbs de Fairbanks en Alaska. Les trous Ctaient situCs B 22- 150 m de distance les uns des autres. Des phoques attach& sans bandeau sur les yeux rbussissaient B localiser les trous lorsque le hasard les menait assez prbs des trous pour qu'ils puissent les voir. Lorsquils avaient les yeux band&, les phoques rCpondaient B des signaux acoustiques. La sensibilitC tactile des vibrisses Ctait utilisCe par les phoques aux yeux bandCs dans le voisinage immdiat d'un trou dCjB repCrC par un signal acoustique. Les rkactions d'un phoque juvCnile Ctaient sensiblement les memes que celles d'un adulte de la meme espkce ou d'un Phoque commun adulte. Les rCsul- tats indiquent que les phoques utilisent une hiCrarchie sensorielle pour repCrer les trous de respiration : la vision, l'audition et la sensibilitk des vibrisses. Le rythme cardiaque a CtC mesurC au cours de plongCes volontaires chez le Phoque annelC le plus jeune B 1'8ge de 2 ans et B l'fige de 3 ans. I1 se produit une importante bradycardie de plongCe, ce qui semble indiquer que les phoques de taille relativement petite font communCment appel B une rkaction de plongCe bien Ctablie au cours des excursions sous la glace.

[Traduit par la revue]

Introduction Some seal species, such as the arctic ringed seal (Phoca

hispida) and the antarctic Weddell seal (Leptonychotes wed- delli) exist in polar marine environments that are dominated by a nearly continuous cover of sea ice. Other species, spotted seals (Phoca largha), for instance, spend several months of the year in regions of pack ice varying in cover from dense to loose. They all require ready access to breathing holes or open leads for reaching the surface.

Polar marine mammals native to shore-fast ice habitats are capable of precise pilotage from one breathing hole to another while swimming under a continuous expanse of sea ice. Much of the evidence is of an anecdotal nature, and relatively few experimental studies have been performed. Some extra- ordinary feats of navigation by Weddell seals have been reported (Kooyman 1968, 198 1). Individuals of this species have shown the ability to return to a given breathing hole after

excursions during which they had traveled 2 km or more under sea ice 2 m thick. Little is known about their route during such excursions, beyond the observation that within 100 m or so of the breathing hole they departed and returned along similar paths (Kooyman 198 1).

The favored habitat of ringed seals throughout the year is sea ice. They are circumpolar in distribution and extend north- ward from the southern seasonal boundary of sea ice. They exist principally in shore-fast ice or in extensive areas of continuous large ice floes. Ringed seals maintain breathing holes by abrasion of the ice with the claws of their foreflippers. These holes are often located along pressure ridges or refrozen leads where holes are first made during freeze-up and are maintained during the advancing winter season (McLaren 1958; Smith and Stirling 1975; Smith 1987). The winter habitat of spotted seals is the southern margins of pack ice in the Bering Sea (Burns 1970). They seldom, if ever, need to maintain breathing holes, but they are likely to require the

'Contribution No. 730, Institute of Marine Science, University of ability to recognize local and changing under-ice topography. Alaska Fairbanks, Fairbanks, AK 99775- 1080, U. S . A. The sensory modalities used by marine mammals for orien-

hinted in Canada 1 Imprimt au Canada

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ELSNER I ET AL. 2507

tation and navigation have not been well studied, owing to the difficulties of investigating such characteristics in the animals' natural habitats. What little is known suggests that vision and hearing are important to this ability. Laboratory studies have shown that pinniped visual sensitivity is highly developed (Watkins and Wartzok 1985). Even so, vision is not always sufficient in natural habitats where light levels are low and water turbidity is high. The importance of vision is suggested by the observation that under-ice mobility and diving depth of Weddell seals are inhibited by darkness (Kooyman 1975).

Hearing is another important source of information in the underwater environment. Harbor seals (Phoca vitulina) have been shown to be able to identify the directional source of underwater sound to within 3" (Mohl 1968), and they were able to locate the source of pulsed signals more efficiently than they could those of steady origin (Terhune 1974). Several experimental attempts have been made to determine whether or not seals and sea lions have the ability to use echolocation in pursuit of prey or experimental targets (Evans and Haugen 1963; Moore 1975; Renouf and Davis 1982). However, echolocation has not been conclusively demonstrated in pinnipeds (Schevill 1968; Schusterman 1975; Wartzok et al. 1984). Nevertheless, the recognition that blind pinnipeds in healthy condition are occasionally encountered (Poulter 1968) suggests that vision is not absolutely necessary for survival.

Pinniped adaptations to habitats in continuous ice cover are represented in the Arctic and the Antarctic by ringed seals and Weddell seals, respectively. Both species maintain breathing holes in similar ice conditions and must depend upon easy and regular access to them. However, the two species differ in behaviour and exposure to predation (Stirling 1974). The small ringed seal contrasts markedly with the larger Weddell seal, and they also differ in diving capability. Maximum dive durations are about 18 min for ringed seals (Ferren and Elsner 1979) and over 1 h for Weddell seals (Kooyman 198 1). There- fore, differences might be expected in the physiological responses shown by these species in their successful adaptations to the sea ice environment.

We have addressed the following question: What sensory information is used by seals to locate distant breathing holes? This study was designed to test the ability of two captive arctic pinniped species, spotted seals and ringed seals, to find their way between breathing holes drilled in the ice of a frozen pond. The experimental plan was to test the animal's use of vision, hearing, and the vibrissal sense as possible contribu- tors in determining the location of the artificially prepared breathing holes. The relative contribution of each of these sensory modalities was tested in conditions involving the selec- tive, benign, and reversible impairment of senses or the artificial production of cues. Some preliminary results of these studies have been reported (Sonafrank et al. 1983; Wartzok et al. 1987).

Methods The experiments were performed near Fairbanks, Alaska, in a

man-made pond created for the excavation of gravel. The pond is roughly circular, 300 m in diameter, and 8 - 10 m deep. Ice ranged from 30 to 80 cm in thickness and was covered by 20-40 cm of snow. Under the ice the pond water was still and turbid. The pond has a homogeneous bottom of gravel and mud. An additional trial was undertaken in a larger lake.

In the first two seasons of this study the experimental animal was a young male spotted seal, body weight 40 kg, native to the Bering

Sea. During the third, fourth, and fifth season these studies were con- tinued using two ringed seals, one an adult male which was captured at Barrow, Alaska, and the other a male pup found abandoned on the beach at Nome at an age of 2 or 3 months. When used in these studies, it was 2 and 3 years of age and weighed 30-45 kg. The adult was estimated to be at least 8 years of age, judging by the count of claw annuli, and weighed 65 kg. It is likely that the pup had little previous experience with under-ice pilotage.

The trials consisted of two kinds of experiments: daylight tests, without impairment of vision, compared with similar testing when blindfolded, and tests in which an acoustic cue was provided while vision and (or) vibrissal sense were impaired. The seals were prepared for recovery, should that become necessary, by attachment of a tether consisting of polypropylene line, chosen because of its flota- tion. The tether was attached either to a canvas jacket worn by the seal or to a padded cable encircling the thorax. The seals were blindfolded by a combination of materials, including cloth, neoprene, and bathing cap rubber, and an opening for the nose and mouth was provided. Vibrissal restriction was obtained by containing the vibrissae flat against the face within the blindfold or by covering them with a stocking pulled over the head.

Three to six holes, approximately 75 cm diameter, were drilled 22 - 120 m apart in the ice of the experimental pond, 150 m apart in the lake. Patterns of breathing holes used in the five seasons are shown in Fig. 1. The seals were allowed time, half an hour or more, to become accustomed to the situation and to perform whatever exploratory dives they wished. The seal's behaviour while swimming without sensory impairment but loosely tethered consisted of frequent dives and spontaneous under-ice exploration. This voluntary diving allowed the seal to control the frequency and duration of dives. When blindfolded, the seal remained close to the entry hole and was usually unwilling to swim away farther than 1 or 2 m. To test the seal's capability more severely in conditions of sensory impairment, forced diving was used in some experiments. In these instances, a plastic or metal bucket was placed in the seal's entry hole, thus forcing the animal to search for another breathing hole. Diving times up to 16 min 30 s were allowed. If unsuccessful, the seal was returned by the tether to the original entry hole. After such excursions a recovery period amounting to twice the dive duration was allowed.

Determinations were made of heart rate during 83 dives of the juvenile ringed seal by applying surface electrodes consisting of flat copper disks 2 cm in diameter cemented to rubber pads and covered by the canvas jacket. The electrode leads were incorporated into the tether line and connected to a Hewlett Packard electrocardiograph or Biocom FM transmitter.

Results Seals were tested in a total of 481 dives. Of these, 298

lacked sensory restrictions, in 145 the animals were blindfolded and provided with acoustic signals, in 28 they had only vibrissal restriction, and in 10 they had both blindfolds and vibrissal restrictions. Results of 328 dives that resulted in hole finding are summarized in Table 1.

Unrestricted dives We refer here to voluntary dives undertaken without sensory

restriction but with a loosely trailing tether. When the seal was first allowed to enter the initial hole, through which it was introduced to the water, it voluntarily swam away for short distances and returned to the entry hole without difficulty. The excursions increased in duration and distance over the subse- quent half hour or so of familiarization. Nearby holes, those approximately 20 - 30 m distant, were quickly located by the seal, which was apparently depending upon visual cues. This assumes that these holes were within a distance calculated to permit visual detection, based upon laboratory studies (see later). If the hole was more distant, the seal often located it

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TABLE 1. Transits between breathing holes

Distance Blindfold, vibrissal between holes No sensory Blindfold and cover, and acoustic

(m) restrictions acoustic signal Vibrissal cover signal

Spotted seal 22 46 3 3 23 40 28 2 43 2 47 2

Ringed seal Adult

Juvenile

FIG. 1. Locations of artificial breathing holes used in each of five seasons. Arrows point north. A-A and B-B indicate two separate hole location experiments.

while swimming a random pattern which took it incidentally attracted to that site by an acoustic signal. The free running out within a few metres of the hole. The two ringed seals failed of the tether provided rough information about direction and to locate a breathing hole 90 m distant after 17 repeated dives swimming speed. The time of more rapid and direct transits (adult, 6 dives; juvenile, 1 1 dives) lasting up to 16 min, in was measured. A range of speeds, from less than 1 m/s to which the entry hole was blocked. However, they were able bursts of 4 m/s, was determined in this manner. Most transits to do so during hole-finding trials at 23 and 50 m. They later between holes were performed at about 2 m/s. Histograms successfully located the 90-m hole while blindfolded and showing the durations of voluntary tethered dives that lacked

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ELSNER ET AL. 2509

251 VOLUNTARY DIVES RINGED SEAL

69 VOLUNTARY DIVES

DIVE DURATION (MIN)

FIG. 2. Frequency and duration of voluntary dives by (A) a young ringed seal and (B) a spotted seal.

sensory restrictions, 69 by the spotted seal and 251 by the dives by the ringed seal, 92% lasted less than 6 min. Its long- younger ringed seal at 2 years of age, are presented in Fig. 2. est voluntary dive was 13 min. Of dives by the spotted seal, Dives resulting in transit to another hole, as well as those in 94% were less than 4 min in duration. Its longest voluntary which the seal returned to the initial hole, are included. Of the dive was 6.5 min.

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To estimate the maximum distance at which light entering a hole could be detected, we determined the light extinction coefficient in the turbid pond water. These values decreased with studies that were performed later in successive seasons: 2.76lm in January, 1.65lm in March, and 0.66lm in April. The sensitivity threshold determined in the laboratory at 515 nm for spotted seals adapted to a light intensity of 0.5 mW mm-2 . nm-I is pW mm-2 nmdl (Wartzok 1979). This intensity is in the range of that experienced on a typical day at the pond during our studies. Under these conditions we estimate that the seal could visually detect the light penetrating a breathing hole from a distance of 7 m in the Janu- ary studies, 12 m in March, and 39 m in the April trials, the variations being accounted for by the increasing solar eleva- tion as the season progressed.

Blindfolding and acoustic signals The blindfolded seals remained close to the entry hole or

swam about in an apparently aimless and random fashion. During our early experiments with the spotted seal, we observed what appeared to be the seal's ability to locate a distant hole while blindfolded and without additional sensory input. However, it soon became clear that we were inadver- tently providing useful acoustic cues at the targeted site by such activities as foot shuffling. When an acoustic signal (tapping on ice, stirring of water) was provided at one of the distant holes, the blindfolded seal in nearly all instances swam purposefully toward that location. We tried a number of acoustic signals at distant holes, including stirring or splashing the water, scratching the ice, and tapping on the side of the hole with wooden or metal rods. Tapping provided an effective and reproducible signal and was used throughout.

Blindfolded seals responded to the site of the tapping signals by swimming, often directly, to that site, positioning beneath the sound source, and then slowly rising to the surface. The maximum distance we have employed in such a test was 150 m with the younger ringed seal. In these trials there was no clear difference in the performance of the spotted seal or the two ringed seals. The juvenile ringed seal sought and located the acoustic signal source with similar speed and ability to those shown by the adult of the same species. Failure to locate the hole from which the tapping signal originated was a rare event; it occurred six times with the juvenile ringed seal at 25 m. Successful hole finding was accomplished in all other trials in which the seals were blindfolded and a tapping signal was used.

Despite our monitoring with a flat-response hydrophone (30 Hz - 20 kHz + 0.5 dB, International Transducer Corpo- ration 6050C, Acoustic Systems Inc. RS307 acoustic monitor, Kudelski S.A. Nagra IV tape recorder) we failed to detect vocalizations or other sound production by the seals.

Vibrissal sense The spotted seal that had its vibrissae restricted but was not

blindfolded showed no apparent decrement in its ability to locate breathing holes at 33 m, the only distance at which this trial was performed. The seal surfaced quickly in the center of the hole. Blindfolded seals with their vibrissae unrestricted surfaced more slowly and were often observed to brush the vibrissae lightly against the ice edge near and within the targeted hole while surfacing. This behavior contrasted with that of seals without sensory impairments, which surfaced promptly and without hesitation. The blindfolded animal that was also impaired by vibrissal restriction responded readily to

a distant ice-tapping signal. However, it appeared to be slower in locating the precise position of the hole.

Heart rate Heart rates were recorded on the younger of the two ringed

seals during pilotage experiments performed when it was 2 and 3 years of age. It responded to these dives with a profound bradycardia, resulting in rates as low as 10 beats per minute (bpm) or less (Fig. 3). Heart rate was determined without blindfold (70 voluntary dives, 17 s to 5 min 20 s duration) and with blindfold and provision of an acoustic tapping signal at a remote breathing hole (13 dives, 1 min 30 s to 16 min 30 s), all showing heart rates of frequently less than 10 bpm. Anticipatory increases in heart rate were seen in the nonblindfolded seal when approaching a breathing hole (Fig. 4), but the blindfolded seal did not display similar anticipatory tachycardia before its nostrils emerged at the surface. On two occasions the voluntary diving seal without blindfold was observed to emerge briefly and take small breaths without increasing its heart rate.

Discussion Field observations by Smith and Stirling (1975) indicate that

the distances between our artificial holes are within the range of those seen in the natural sea ice habitat of ringed seals. Along one refrozen lead of 9.7 krn they counted 34 breathing holes. Distances between adjacent holes measured 27 -563 m. The maximum distance between adjacent breathing holes measured could be transited well within the dive durations observed in our experiments.

The type of orientation involved in location of breathing holes in this study most nearly approximates the type 1 category defined by Griffin (1955), which should be described as pilotage rather than true navigation in unfamiliar territory. Pilotage, as distinguished from navigation or compass orientation, is goal finding by reference to familiar landmarks. Ran- dom searching until such landmarks are identified is also included in this category.

Our results suggest that seals in their natural habitats make use of under-ice topography and other local cues for main- tenance and extension of familiarity within an under-ice territory, even a changing one. Freshwater lake ice is relatively smooth and uniform compared with sea ice, which has a dis- tinct topography and appearance, as viewed from below, of pressure-ridge keels, refrozen leads, and irregularities in snow cover. These features can be expected to provide "territorial landmarks" to the seal in whose habitat they occur.

The primacy of vision in the detection of new breathing holes was indicated by the relation between the apparent detection distance and the distance at which the seals were expected to be able to first see the holes, based on laboratory- determined visual sensitivity (Wartzok 1979). Hobson (1 966) pointed out that even in apparent darkness some light is avail- able to an underwater eye looking upward, against which con- trasting objects may be discernible. When even a small amount of light is present, vision is likely to be the dominant sense. As light decreases, acoustic cues can provide a supplementary source of information about the environment. Within a shorter range, especially in circumstances in which touch is involved, vibrissal distortion will add another dimension.

Harbor seal auditory sense can detect frequencies from 1 to 22.5 kHz in air and 1 to 180 kHz in water. The region of highest sensitivity is 32 kHz in water and 12 kHz in air (Mohl

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Time (min)

FIG. 3. Heart rate of young ringed seal during voluntary dives. Solid line above record indicates submergence.

Time (min)

FIG. 4. Heart rate of young ringed seal during voluntary dive. Arrows indicate start and end of dive.

1968). Ringed seals have a basically flat (f 7 dB) underwater sensitivity in the frequency range of 1-45 kHz, with highest sensitivity at 16 kHz (Terhune and Ronald 1976). Our monitoring equipment was flat to 20 kHz and therefore should have been able to detect those vocalizations to which the seal was most sensitive.

Some pinniped species produce click trains. Harbour seals have been reported to increase the production of clicks in decreased light levels (Renouf and Davis 1982), although click train vocalization in spotted seals is related to the reproductive cycle rather than to light levels (Gailey-Phipps et al. 1983).

Steller sea lions and harbour seals have been reported to be able to capture live fish in darkness, producing clicks while doing so (Poulter and Del Carlo 1971; Renouf and Davis 1982). In experiments with California sea lions (Evans and Haugen 1963; Schusterman 1967) and gray seals (Oliver 1978; Scronce and Ridgway 1979) no evidence for echolocation was demonstrated. If seals were to successfully employ echolocation for pilotage to breathing holes in their natural habitat, it would require a return signal from a hole of about 30 cm in diameter and located at the surface of a cone-shaped tunnel in ice sometimes 2 m thick.

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Schusterman (1975) has suggested that sea lions may orient to the low-frequency sounds emitted by some fishes and invertebrates. In the experiments reported here we were impressed by the immediacy with which the seals responded to the onset of the distant acoustic signal produced by tapping on the ice, even in the absence of prior training or accustom- ization. The significance to the seal of the tapping, produced by either wooden or metallic rods, is quite unknown. We are at a loss to explain why the animal should associate it with the location of a breathing hole. It is quite likely, however, that holes in the ice are sources of ambient noise and thus provide strong sensory inputs. The loud, sharp sound produced by the tapping is the type that can be most easily localized (Terhunel974) and we suspect that the blindfolded seal is will- ing to investigate any clearly discernible sound source. The hole to which the animal was directed by acoustic cues was on several occasions set at a location previously unused by the seal, which practice presumably excluded the possibility that the seal could obtain cues of direction and distance from some other source.

Pinniped vibrissae are well developed and densely inner- vated (Dykes 1975). Harbour seals are capable of detecting vibrations between 5 and 1000 Hz with vibrissae, although sensitivity responses determined behaviorally (Renouf 1979) are at variance with those determined neurophysiologically (Dykes 1975). The ability of four harbor seals to capture fish in murky water was little affected by removal of their vibrissae (Renouf 1980).

The physiological effect of these dives is suggested by the frequency data of free dives, which show that 92 % of those by the juvenile ringed seal lasted less than 6 min. A similar pattern of free dives was noted in the adult spotted seal. The longest free dives were 6 min 10 s for the spotted seal, and 13 min for the juvenile ringed seal. Adult spotted seals are able to dive for about 20 min (Elsner and Gooden 1983). Several lines of evidence suggest that the usual aerobic diving limits of the smaller phocid seals, such as harbor, spotted, and ringed seals, are approximately 8 - 10 min (Scholander et al. 1942), while those of adult Weddell seals are 18 min (Kooyman et al. 1980). Thus, while the requirements for under-ice excursions might be expected to be of a generally similar nature for both ringed and Weddell seals, the physiological demands upon ringed seals would accordingly be potentially more severe.

Diving bradycardia is a well-established and thoroughly studied response to diving episodes in seals. It is also recog- nized that the reduction of heart rate during free, nonforced dives is usually less profound, resulting in a more modest bradycardia in such situations (Elsner 1965; Kooyman 1981; Hill et al. 1987). Heart rate is therefore a physiological indica- tor of the severity of the dive. The extreme bradycardia noted during voluntary dives in the ringed seal in these studies indicates a considerably more potent invocation of the diving response than that ordinarily seen in free-diving seals. Com- parison with the more modest bradycardia seen in under-ice free-diving Weddell seals (Hill et al. 1987) suggests that such dives pose a substantially greater threat to the relatively small ringed seals. Presumably they prepare for a dive of unpredict- able duration by making maximum use of protective reactions.

Acknowledgments We thank the many persons who contributed to the success

of this project. Shelli Clay, Pam Croom, Randall Davis,

Gregory Finstad, Juan Goula, Wayne Grinder, Jay Johnson, Anna Larsen, Jonathan Lewis, Gil Mimken, Mary Moore, Jeffrey Nester, Jay Quakenbush, Lori Quakenbush, John Sease, Louise Smith, John Smithhisler, Una Swain, Kathy Turco, Donna Warnick, Wendy Warnick, Lori Wickham, and Steven Winch assisted with various aspects of this study. Dr. Robert Dieterich provided veterinary supervision. The Publications Department of the Institute of Marine Science, Fairbanks, University of Alaska, assisted in the preparation of illustrations and manuscript. Funding support was provided by the University of Alaska, Alaska Council on Science and Technology, and the National Science Foundation (DPP research grants 8503371 and 8619272). The seals were captured and used in this study under the terms of National Marine Fisheries Service Marine Mammal permits 3 1 and 543 to R. Elsner.

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HILL, R. D., SCHNEIDER, R. C., LIGGINS, G. C., SCHUETTE, A. H., ELLIOT, R. L., GUPPY, M., HOCHACHKA, P. W., QVIST, J., FALKE, K. L., and ZAPOL, W. M. 1987. Heart rate and body temperature during free dives of Weddell seals. Am. J. Physiol. 253: R344-R351.

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