paralysis as a defence response to threatening stimuli in harp seals ( phoca...
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Paralysis as a defence response to threatening stimuli in harp seals (Phoca groenlandica)
Christian Lydersen and Kit M. Kovacs
Abstract: In this study we describe the behavioural and physiologial characteristics of a fear-induced paralysis response in harp seals (Phoca groenlandica). Of 382 pups tested, 328 (86%) displayed this passive defence response, and of 46 adult seals tested, 26 (57%) individuals exhibited paralysis. Gender had no effect, but among pups there was a signifiant increase with age in the proportion of individuals that performed the response (contingency table; G = 21.46, p = 0.002). During paralyses seals became rigid, the foreflipprs were brought into the sides of the body, the hind flippers were pressed closely together, and the neck was retracted so that the forehead was drawn into the fat sheath that encases the rest of the body. The animals would always urinate and often defecate. Physiologically speaking, paralyses had two phases. In pups, an apnoea phase preceded a period of hyperventilation. Adults alternated between these two phases more sporadically during a paralysis bout. Mean heart rates of pups during paralysis apnoeas were approximately 30 beatslmin. During the hyperventilatory phase their heart rates escalated to values in excess of 150 beatslmin. Respiration rates for the pups during hyperventilation ranged from 26 to 66 breathslmin. Heart rates of adults during apnoeas were more viable than those of pups, but the average value was similar (32 beatslmin). The lowest heart rate recorded was 10 beatslmin. Average heart rates of adults during breathing phases were lower than those of pups, ranging from 118 to 130 beatsjmin. A suite of lactation-related adaptations and ecological circumstances may explain the paralysis response in harp seals. Harp seals have evolved in the presence of polar bears. They are afforded some protection by giving birth in dense aggregations on unstable ice that is variable in geographical location, but pups are extremely vulnerable when a surface predator does enter the whelping patch, and available defence options are limited. The paralysis response may serve to disinterest the predator and so reduce the risk of incidental injury from traumatic, playful handling by a predator by protecting vital body parts.
RCsumC : On trouvera ici la description des caracteristiques Cthologiques et physiologiques d'une paralysie provoquCe par la peur chez des Phoques du Groenland (Phoca groenlandica). De 382 petits examinks, 328 (86%) ont manifest6 cette rkaction de dCfense passive et des 46 adultes expkrimentaux, 26 (57%) ont Cgalement manifest6 la rCaction de peur. I1 n'y a pas de diffkrences entre miles et femelles, mais la proportion d'individus affectis augmente significativement en fonction de l'ige chez les animaux immatures (tableau de contingence; G = 21,46, p = 0,002). Durant la paralysie, les phoques deviennent rigides, leurs nageoires antkrieures sont collCes aux cBtCs du corps, les nageoires caudales sont collCes l'une sur l'autre et le cou est retract6 de f a ~ o n h faire disparaitre le front dans la couche de graisse qui enveloppe le reste du corps. Les phoques urinent et mCme dCfequent souvent. La paralysie comporte deux phases physiologiques. Chez les immatures, une phase d'apnCe prCckde une pCriode d'hyperventilation. Chez les adultes, ces deux phases se produisent en alternance, plus sporadiquement. Le rythme cardiaque moyen d'un petit durant la phase d'apnCe a CtC CvaluC h environ 30 battementslmin; durant la phase d'hyperventilation, son rythme cardiaque grimpe jusqu'h plus de 150 battementsjmin et son taux respiratoire va de 26 h 66 respirationslmin. Le rythme cardiaque des adultes durant les phases d'apnCe est plus variable que celui des petits, mais le nombre moyen de battements par minute est semblable (32). Le rythme cardiaque le plus faible enregistrC a CtC de 10 batternentslmin. Durant les phases respiratoires, le rythme cardiaque des adultes est plus faible que celui des petits (1 18 - 130 battementsjmin). Une sCrie d'adaptations reliCes ii l'allaitement, combinCes h des conditions Ccologiques sont peut-Ctre responsables de la paralysie observCe chez les phoques. Les Phoques du Groenland ont CvoluC en prCsence d'Ours blancs. 11s sont partiellement protCgCs par leur habitude de mettre bas en groupes nombreux sur des glaces instables dont la position gkographique varie, mais les
I Received May 4, 1994. Accepted ~ovember 2 1, 1994.
I C. Lydersen. Norwegian Polar Institute, P.O. Box 399, N-9001 Tromso, Norway. K.M. Kovacs. Department of Biology, University of Waterloo, Waterloo, ON N2L 2G1, Canada.
Can. J. Zool. 73: 486 -492 (1995). Printed in Canada / Imprime au Canada
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petits sont extremement vulnCrables lorsqu'un prCdateur de surface envahit le territoire de mise bas, parce que leur systkme de dCfense est trks limit& La reaction de paralysie peut servir a dCsintCresser le prCdateur et a protCger les parties vitales des phoques en rCduisant les blessures qui rCsultent de la manipulation traumatique du prCdateur qui s'amuse avec sa proie. [Traduit par la RCdaction]
Introduction became rigid, with the neck pulled in and the flippers held
When animals are exposed to frightening stimuli they generally either defend themselves, run away, or remain still to avoid detection. The first two options are forms of active defence that are commonly referred to jointly as the "fight or flight" response (Cannon 1929). This response type is associated with a well-defined set of physiological adjust- ments that is controlled principally by the sympathetic part of the autonomous nervous system (Gabrielsen and Smith 1994). These physiological adjustments, which involve increases in heart rate, respiratory rate, metabolism, skeletal muscle blood flow, and blood sugar levels, prepare an animal for surviving an encounter with a predator either by fighting or by avoiding contact. The alternative option is a passive defence response that also involves a well-defined set of physiologi- cal adjustments that is controlled principally by the para- sympathetic part of the autonomous nervous system. These adjustments are opposite to those involved in the active defence response and include apnoeas, bradycardia, and peripheral vasoconstriction (Gabrielsen and Smith 1994). Two forms of passive defence responses are commonly recog- nized, freezing and paralysis. Freezing is normally a response to mild stimulation. Paralysis is a more extreme response and is usually associated with stronger stimulation. During freez- ing an animal becomes motionless and if the threat disap- pears, its heart and respiratory rates rapidly return to normal predisturbance levels. If the stimulus does not disappear, but becomes stronger, the animal can either display an active defence response, such as the flushing-flight of willow ptar- migan hens (Lagops lagopus) (Steen et al. 1988), or display a fear-induced paralysis reflex, such as that of the American opossum (Didelphis marsupialis) (Gabrielsen and Smith 1985). If captured by a predator after a flight attempt, an animal may also then display a paralysis response. During paralysis animals normally show more profound bradycardia than dur- ing freezing and also frequently urinate or defecate. The anti- predator value of the paralysis behaviour lies in the fact that predators often lose interest in immobile animals (Gallup et al. 197 1 ; Gabrielsen and Smith 1985), particularly if their hunger has already been satiated.
Most species are capable of displaying either active or pas- sive defence responses, depending on the situation (Gabrielsen and Smith 1994); they have the physiological capacity for both options. In some species age is a factor that determines the type of response displayed. This is illustrated quite pro- foundly in white-tailed deer (Odocoileus virginianus), where young fawns tend to display a freezing response when threat- ened, while older fawns, which are better developed neuro- muscularly, tend to flee (Jacobsen 1979).
Harp seal (Phoca groenlandica) pups approached or touched by human beings and adult harp seals that are cap- tured often display paralysis. This behaviour was docu- mented by Ronald et al. (1970), who said that the animals
tight against the body; the nostrils remained closed but the eyes were able to follow movements of the observer. These researchers obtained electrocardiograms (ECGs) from a 3-day- old pup and an adult, which demonstrated a reduction in heart rate from 200 and 90 to 15 and 5 beatslmin for the pup and adult, respectively. In the present study we tested how common this passive defence response is in different age groups of harp seals, and we describe the physiological con- dition of paralysis in different age groups more completely in terms of heart and respiratory rates.
Material and methods
This study was conducted in a whelping patch of harp seals in ,the drifting pack ice in the Gulf of St. Lawrence, Canada. The patch was located by helicopter approximately 70 km north of Isles de la Madeleine. Data were collected on 9, 1 1, and 12 March 1994.
White-coated harp seal pups of different ages were approached and their behaviour was recorded. The responses of individual pups were classified into three categories: (I) spontaneous paralysis: the response was triggered by our presence; (2) induced paralysis: the response was triggered only after the animal was touched by one of us, most often in the facial area; (3) no passive defence response: we were unable to bring the animal into paralysis even after touching and manipulating it for about 15 s.
The pups were aged according to the stages described in Kovacs and Lavigne (1985), where the average age of yellow coats, thin white coats, fat white coats, and grey coats is 1, 3, 7.5, and 12 days, respectively.
The behaviour of adult harp seals was classified in the same manner as for pups. However, if paralysis was not displayed spontaneously, ,the adults were netted to determine whether a response could be induced.
The heart rates and breathing frequencies of the harp seals were monitored during paralysis. These experiments were performed on pups of different ages and on adults of both sexes. An animal was first brought into paralysis and then carried (or hauled in the case of adults) into the lee of an ice hummock, where the measurements were conducted. Heart rates were measured using a Cardioline ETA 150 electro- cardiograph (REMCO ITALIASPA, S. Pedrino di Vignate Milano, Italy). An electrode was placed under each fore- flipper and the signals were printed with a hot pen on the thermoreactive paper with a paper speed of 25 mm . s-I (f 2 %). While monitoring ECG signals one observer watched the nostils of the seal, and when a breath occurred a mark was placed on the electrocardiogram trace. This allowed us to simultaneously collect breathing frequencies, apnoea inter- vals, and heart rates. These measurements were taken manu- ally from the ECG trace. Heart rate was measured as the distance between subsequent R - R intervals.
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Table 1. Results from testing harp seals for the paralysis response.
Response (%)
No passive Age category N Spontaneous Induced response
Yellow coat 20 25 55 20 Thin white coat 99 34 44 2 1 Fat white coat 164 50 3 7 13 Grey coat 99 6 1 33 6
Adult female 4 1 7 46 46 Adult male 5 0 80 20
Note: "Spontaneous" refers to a response triggered simply by human approach; an "induced" response refers to the same reaction being performed only after the animal was touched. The average age of yellow, thin white, fat white and grey coats is 1 , 3, 7 .5 , and 12 days, respectively (Kovacs and Lavigne 1985).
Results
Harp seal pups that did not display spontaneous paralysis upon approach always displayed an active defence response, usually by trying to crawl away. Animals that tried to crawl away and did not go into paralysis when touched sometimes tried to defend themselves biting or scratching with the fore- flippers. However, most pups and more than 50% of the adults did enter paralysis (Table 1). In this state the whole body became rigid. The foreflippers were brought tight into the sides of the body and the hind flippers were pressed closely together. The neck was retracted so that the head was drawn into the fat sheath that covers the rest of the body. The eyes were initially kept tightly shut but gradually opened if the animal was not touched, although the rest of the posture was maintained. The animals always urinated and would often also defecate.
Out of 382 pups tested, 328 (86%) displayed the paralysis response (Table 1). Within this group, 181 displayed the response spontaneously and 147 exhibited induced paralysis. There were no differences between the sexes in the frequen- cies of the different responses among harp seal pups (contin- gency table; spontaneous: G = 5.09, p = 0.17; induced: G = 4.19, p = 0.25; no reaction: G = 0.87, p = 0.88). A significant increase in spontaneous and induced paralysis was found with increasing age in the pups (contingency table; G = 21.46, p = 0.002). Out of 46 adult seals tested, 26 (57%) displayed the paralysis response. However, only three adult females and no adult males showed spontaneous paralysis (Table 1).
In pups the paralysis state had two distinct phases, apnoea followed by a period of hyperventilation (Fig. 1). Adults alternated between these two phases more sporadically (Fig. 2). The mean heart rate during paralysis apnoeas of a yellow coat, a thin white coat, and a fat white coat was 30 + 6,28 f 10, and 33 + 12 (SD) beatslmin (Fig. 2), with minimum values of 21, 13, and 17 beatslmin, respectively. During breathing periods in paralysis, the pups normally hyperventilated and the heart rates of the three pups escalated to average values of 171 + 38, 156 f 24, and 150 f 25 beatslmin, respectively; respiration rates for the pups dur- ing this phase were 66,40, and 26 breathslmin, respectively. Both the thin and the fat white coats performed a single venti-
lation, then resumed apnoea prior to commencing hyper- ventilation. However, the yellow coats performed a relatively long apnoea followed by an intense hyperventilatory phase and did not go back into apnoea during the measurement period, which was about 2 min longer than is illustrated in Fig. 2.
The heart rate of adult harp seals during apnoeas was 44 f 8 beatslmin for the male and 17 + 6 beatslmin for the female, with minimum recordings of 20 and 10 beatslmin, respectively (Fig. 2). The heart rate during breathing phases was 130 + 54 beatslrnin for the male and 1 18 + 33 beatslmin for the female. The male performed single ventilations when he broke the state of apnoea, whereas the female performed multiple breaths. The respiratory rate of the female during bursts of breathing was much lower than those measured for the pups, varying between 12 and 18 breathslmin.
Discussion
The paralysis posture displayed by harp seals is very similar to that assumed by other mammals during this type of passive response. The only observed difference was that in harp seals the eyes were closed tightly when the posture was first assumed. In most species, animals in paralysis keep their eyes open and remain visually alert. The initial closure of the eyes in harp seals may simply be due to the very tight con- traction of the head into the fat sheath, which may force the eyelids closed. As the posture is retained over time, harp seals do open their eyes and follow movements in the manner described for other species during fear-induced paralysis.
The general pattern of alternating heart and breathing rates observed among harp seals in the state of paralysis is not restricted to the fear response in these animals. The nor- mal breathing pattern for seals on land is a rhythmic pattern with a small number of breaths separated by apnoea intervals with bradycardia during apnoea and tachycardia during breath- ing (Irving 1939). The apnoea periods observed on land are found to be similar to those during voluntary diving (Kenny 1979), and bradycardia during diving and periods of apnoea on land are significantly different (Pische and Krog 1980). Forced submersion has been found to produce a more pro- found bradycardia than that which takes place during rela- tively shallow voluntary diving (Elsner 1965; Casson and Ronald 1975; Harrison and Ridgway 1975; Hill et al. 1987). Similarly, on land, other frightening stimuli, such as shout- ing in the ear of a blindfolded seal, produce bradycardia like those produced by forced submersion (Scholander 1940). Thus, fear in general seems to produce physiological responses similar to the diving response in seals.
For young phocid seal pups the terrestrial breathing pattern while they are awake is a normal mammalian pattern (Kenny 1979; Lyamin et al. 1993). The periodic pattern, which includes apnoeas, develops with increasing age (Kenny 1979). However, when sleeping on land, even young pups of harp seals and northern elephant seals (Mirounga angusti- rostris) show a periodic breathing pattern (Blackwell and Le Boeuf 1993; Lyamin et al. 1993), with a corresponding brady- and tachy-cardia (Lyamin et al. 1993). Sleep apnoea is thought to be a means of conserving energy and water; the metabolic rate reducing the physiological responses associ- ated with the dive response acts together with the nasal
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Fig. 1. Heart and respiration (+) rates during apnoea and hyperventilation in harp seal pups during paralysis. (A) Yellow coat. (B) Thin white coat. (C) Fat white coat.
0 0 30 6 0 90
Time (s) countercurrent heat exchanger (Blackwell and Le Boeuf 1993). Submersion-induced bradycardia is also evident in new- born northern elephant seals, although they do not enter the water until they are several weeks old under normal condi- tions (Hammond et al. 1969). Based on heart-rate recordings from mother harbour seals (Phoca vitulina) and their fetuses, it seems that the regulatory mechanisms which determine apnoea bradycardia actually develop prior to birth, during the foetal stage (Bacon et al. 1985). Thus, it seems that phocid seal pups are physiologically capable at birth of responding to different situations with apnoeas and bradycardia, but for young pups that do not enter the water until after the nursing period, the normal on-land breathing pattern when they are awake is a regular one.
In the present study, we recorded heart rates and breath- ing frequencies in harp seals only during paralysis. Normal, undisturbed values for these parameters were measured in 10-day-old and 1-month-old individuals of this species by Lyamin et al. (1993). When pups were awake, resting in the snow, their breathing was regular, at a rate of about 17 breaths1 min, and their heart rate was 106 f 4 beatslmin. However, during sleep the pups performed apnoeas that lasted up to 140 s, which alternated with intervals of hyperventilation, when the breathing rates were about 23 breathslmin. During the apnoeas their heart rates were about 70 beatslmin and during hyperventilation they were about 11 1 beatslmin. In our study, pups in the state of paralysis performed brady- cardia, with heart rates that dropped from 150 - 171 to 28 -
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Fig. 2. Heart and respiration (+) rates during apnoea and hyperventilation in adult harp seals during paralysis. (A) Male. (B) Female.
400
Time (s) 33 beatslmin, and extreme rates of hyperventilation, i .e., more than 1 breathls. These values far exceed those for nor- mal sleep. Ronald et al. (1970) measured the heart rate of one 3-day-old harp seal pup during paralysis and found a reduction from 200 to 15 beatslmin. These results are similar to ours and neither is surprising, since fear appears to pro- duce deeper bradycardia than that which occurs during nor- mal diving or sleep (see above). Although this fear response appears to be extreme it does not approach the physiological limits for seals in terms of the reduction in heart rate. During long voluntary dives seals can show profound bradycardias that are much more extreme than those found during routine diving or those observed during fear responses. In extreme cases of voluntary natural dives, heart rates as low as 4 beats1 min have been recorded (Thompson and Fedak 1993).
In our study, hyperventilation by harp seals during paraly- sis was most extreme in the 1-day-old yellow coat. This pup was brought into paralysis and moved into the lee of some ice hummocks, electrodes were attached, and the instrument was tested before the actual measurement started (as was the case for all of the study animals). Thus, 3 -4 min passed dur- ing which the pup was in apnoea before the recordings shown in Fig. 2 started. Once hyperventilation began in this pup, it did not return to apnoea even though the paralysis posture was maintained. The pup's oxygen stores were probably completely depleted by the end of the first recorded apnoea, resulting in the observed breathing pattern. The breath-holding
capacity of a 1-day-old pup is probably quite limited. The older pups involved in this study did take single breaths and subsequently returned to apnoea and the adults had regular alternating periods of apnoea and breathing.
The significant increase in the proportion of harp seal pups that enter paralysis with increasing age is a trend that is also observed in other species. The paralysis response seems to be dependent on higher centres in the brain that can activate parasympathetic parts of the autonomic nervous sys- tem which are not usually fully developed at birth (Gabriel- sen 1986) but appear to become functional during the early neonatal stages. Young opossums do not have the ability to go into paralysis until about the time of weaning (Franq 1969), and in domestic chickens the reaction is found to be virtually absent until they are 7 - 10 days of age (Ratner and Thompson 1960), which corresponds quite closely to their age of physical independence. The development of the pas- sive paralysis defence response is coincident with the period of maximum risk to the neonates of these two species, when they make the transition from maternal care to independent living. Harp seal pups are at serious risk from terrestrial predators only during the nursing and neonatal fasting periods before they commence swimming.
When animals get older and the neuromuscular functions are more fully developed, the passive defence response is often replaced by an active flight response, as seen in calves of a variety of deer species (Jacobsen 1979; Espmark and
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Langvatn 1985). In the present study, only 6.5 % of the adult seals displayed spontaneous paralysis, while the correspond- ing figure for pups was 47.4%.
Paralysis is usually considered to be the final component of a complex sequence of predator -prey interactions (Ratner 1927). When an animal observes a potential predator, a freezing response may be triggered. If the predator continues to approach, the animal will normally try to run away. If cornered by the predator it may try to fight its way out of the situation, and finally, if actually caught it may enter paraly- sis. The antipredator value of the paralysis is that the preda- tor may lose interest in the nonmoving prey item or treat it as if it were dead, and it may get another chance to escape. For example, cats normally do not bite mice when they do not move, and dogs have been shown to lose interest in opos- sums that are in paralysis (Gabrielsen and Smith 1985). In trials where ducks of different species were caught by red foxes (Vulpes vulpes), all ducks went into paralysis and as a result more .than 50% of them escaped the initial capture and handling (Sargeant and Eberhardt 1975), some after being cached by the foxes for later consumption.
Harp seals give birth in large groups in the drifting ice in three geographically distinct populations (Ronald and Healy 1981). All three of these locations are at the edge of the range where polar bears (Ursus maritimus) normally hunt. How- ever, polar bears, which for harp seals are the only surface predator of concern except man, are occasionally reported to enter harp seal breeding grounds in the east of Newfoundland and in the Jan Mayen area. When polar bears enter harp seal whelping patches they can have a serious local impact. Nansen (1925, p. 357) described the behaviour of polar bears in such a situation as follows: "the bears have a rare time with the seal pups, which are an easy prey, as they do not, of course, enter the water until they have cast their woolly covering. The bear will then often play with the pups, as a cat plays with a mouse; it will pick one of them up in its mouth and throw it high up into the air, roll it like a ball over the ice, give it a knock so it tumbles over, and then perhaps take a bite, but leave the little creature half-dead, to begin the same game with another one." According to this description it seems that paralysis in harp seals has antipredator value. While it may induce the bear to leave a pup alone, the posture may have an additional benefit. During paralysis the pups retract their head into the blubber layer that covers the rest of the body, affording their fragile skull some protection from damage during traumatic handling by a predator. The fact that harp seals breed in large colonies is also a general evolutionary antipredator feature. Since predators tend to seize the first individuals they encounter, there is a great advantage for each individual to press toward the centre of the group, a behaviour that leads to the evolution of local aggregations of prey species (Wilson 1975).
Seal pups of other species that have evolved under stronger predation pressure from polar bears, like ringed seals (Phoca hispida) and bearded seals (Erignathus barbatus), do not show any passive defence responses. Ringed seals are born in subnivean lairs that protect them from, among other things, predation (Smith and Stirling 1975), and the pups enter the water and learn to swim and dive while still in their white foetal pelage (Lydersen and Hammill 1993). Pups of bearded seals also enter the water and swim and dive at a
very young age (Lydersen et al. 1994). A paralysis response has never been observed when pups of these two species are handled, nor has this behaviour been documented for pups of other phocid species.
A complex suite of lactation-related adaptations and eco- logical circumstances may explain the occurrence of the paralysis response in harp seals, which is unique among pinnipeds. As northern phocids that spend most of the year in Arctic waters, harp seals have evolved in the presence of polar bear predation. However, compared with Arctic fast ice breeding seals, harp seals are afforded considerable pro- tection during the whelping season by giving birth in dense aggregations on unstable ice that is variable in geographical location and largely inaccessible for polar bears. The short lactation period of only 12 days (Kovacs et al. 1991), achieved through the rapid transfer of milk energy and the concomitant fast growth of harp seal pups, may also serve to reduce mortality by shortening the period when pups are available to surface predators and when females are tied to a fixed location. Female harp seals spend a considerable amount of time away from their pups, in the water (Lydersen and Kovacs 1993), and are thus unlikely to be taken by a sur- face predator. However, the pups are extremely sedentary and do not swim prior to weaning. Both of these characteris- tics are likely important for energy retention and relocation by their mothers in the patch. However, these adaptations that promote efficient energetics make individual pups extremely vulnerable when a predator does enter the whelp- ing patch. The options available to a harp seal pup, or adult, confronted with a polar bear on the ice are limited. The paralysis response may serve to disinterest the predator, which has been satiated through eating other members of the group, and it may reduce the risk of incidental injury from traumatic, playful handling by a predator by protecting vital body parts.
Acknowledgements This study was funded by the Norwegian Fisheries Research Council, the North Atlantic Treaty Organization Interna- tional Scientific Exchange and Collaborative Research Grants Program (Grant No. 92 1216), and the Natural Sciences and Engineering Research Council of Canada. We also thank M.O. Hammill for extensive logistics support and for com- menting on the manuscript.
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