Arteriovenous Anastomoses in the Skin of Seals II. THE CALIFORNIA SEA LION ZALOPHUS CALlFORNlANUS AND THE NORTHERN

FUR SEAL CALLORHINUS URSlNUS (PINNIPEDIA: OTARIIDAE)

M. M. BRYDEN AND G. S. MOLYNEUX School of Anatomy, Uniuersity of Queensland, St. Lucia 4067, Australia

ABSTRACT The structure, distribution and density of arteriovenous anas- tomoses (AVAs) were studied in body and flipper skin of a California sea lion and a northern fur seal. In both animals AVAs consisted of arterial, intermedi- a t e and venous segments, and were generally larger and more tortuous in the sea lion than in the fur seal. In the sea lion the majority of AVAs (72%) oc- curred in the deeper region of the dermis, and the density was significantly greater in the flippers than in the body. In the northern fur seal most AVAs (76%) occurred in the superficial region of the dermis; the density of AVAs in flipper skin was significantly higher than in body skin, and the density in the hind flipper was significantly greater than in the foreflipper.

Arteriovenous anastomoses are important in the regulation of body tempera- ture in seals; when these animals are on land, AVAs function to dissipate body heat, and vascular thermoregulation occurs in the flippers but not over the gen- eral body surface. Due to differences in distribution and density, AVAs play a more significant role in thermoregulation in the northern fur seal than in the California sea lion.

Arteriovenous anastomoses (AVAs) have not been described in the skin of sea lions or fur seals, although their presence in the latter was suspected and their possible function commented upon by Tarasoff and Fisher ('70).

We have postulated (Molyneux and Bryden, '77) t ha t AVAs in the skin of Weddel seals (Leptonychotes weddelli) and elephant seals (Mirounga leonina) are responsible for signifi- cant loss of body heat when the seals a re on land or ice. This is possible because, in Weddell and elephant seals (family Phocidae), insula- tion is afforded by the extensive subcutaneous blubber layer while the pelage provides little insulation on land and none in the water (Ray and Smith, '68). In contrast, in some members of the family Otariidae, the blubber is less ex- tensive and thinner than in phocid seals but the pelage on the body provides a significant degree of insulation. The hair of the California sea lion is wettable and hence provides no in- sulation in the water, and probably minimal insulation on land, based on a comparison of hair patterns in seals (Scheffer, '64). However the thick underfur of northern fur seals is not wettable, so t h a t the very heavy pelage on the

body of fur seals provides considerable insula- tion against heat loss both in the water and on the land (Irving et al., '62).

Thus the Phocidae have the ability to dissi- pate body heat from the entire body surface when the skin vessels are dilated because these vessels a re superficial to the insulating layer of blubber, whereas in fur seals the in- sulating layer of underfur is superficial to the skin vessels and significant heat dissipation from the entire body surface is not possible. However, the flippers of Otariidae are rela- tively large and almost free of hairs, so t ha t heat loss from them is possible (Irving e t al., '62).

In this study we have examined the body and flipper skin of two otariid species: the California sea lion Zalophus californianus which lives off the coast of Mexico and Califor- nia, but ranges as far north as British Colum- bia; and the northern fur seal Callorhinus ursinus which ranges through the Bering Sea and North Pacific Ocean, and during summer hauls out on the Pribilof Islands and other

Received Apr. 15, '77. Accepted Dec. 8. '77.

ANAT. REC. (1978) 191: 253-260. 253

254 M. M. BRYDEN AND G. S. MOLYNEUX

places. Both species spend, without apparent discomfort, at least part of their lives in water t h a t may be up to 40°C colder than their body temperature. Because heat loss from the body surface in air is approximately 50 times less than in water, i t is obvious tha t overheating could be a problem in these animals when they are on land. Both these species have been shown to exhibit signs of heat stress on land (Bartholomew and Wilke, '56; Peterson and Bartholomew, '67). This paper describes the skin vasculature in these two species, par- ticularly the structure and distribution of AVAs, in relation to temperature regulation.

MATERIALS AND METHODS

Tissue collection and preparation One sub-adult male sea lion and one sub-

adult male fur seal were used in this study. The specimen of 2. californianus had been a performing animal at Marineland of Australia (no longer operational) for three years, having been captured in California as a juvenile and flown to Australia in 1972. After i t died the sea lion was frozen, thawed, and then

embalmed with 10% formalin. The specimen of C. ursinus was a n animal which had been killed in the 1975 commercial sealing activity at the Pribilof Islands.

Full thickness skin samples approximately 2 x 3 cm were removed from the dorsal mid- line and the flippers of both animals, and immersed in 10% neutral buffered formalin. Serial sections (10 p ) were prepared and stained with haematoxylin and eosin.

Examination Arteriovenous anastomoses were counted

by following each from i t s arterial origin through its intermediate segment and where possible, to i t s venous termination. In few in- stances, the veins were collapsed and difficult to observe. Each AVA was entered on a dia- gram of the skin sections to ensure tha t it was counted only once.

The distribution of AVAs was recorded in the superficial dermis, the deep dermis and the hypodermis. In this study the superficial dermis is defined as the region extending from the papillary layer to the sebaceous gland

TABLE 1

Distribution and density ofAVAs in the dermis and hypodermis o f a subadult sea lion, 2. californianus and a subadult fur seal C . ursinus. Each figure showing the distribution is the number o f A VAs

expressed as a percentage of the total number of A VAs in the skin sample

Distribution

Animal Dermis AVA density

Region Superficial Deep Hypodermis Nolcm'

Zalophus Dorsal midline californianus

Zalophus Foreflipper californianus

Zalophus Hind flipper californianus

Mean distribution 2 standard

Callorhinus Ventral

Callorhinus Dorsal

Callorhinus Palmar

Callorhinus Web

Mean distribution 2 standard

deviation

ursinus mid 1 in e

ursinus foreflipper

ursinus foreflipper

ursinus hind flipper

deviation

12

25

17

18.0 26.56 79

74

71

82

76.50k 4.93

76

70

71

72.332 3.21 14

20

19

13

16.502 3.51

12

5

12

9.672 4.04 I

6

10

5

7.0 t 2 . 1 6

35 28 80 45

205 261 139 220 211 157 144 195

125 76

805 683 724 760

1,262 1.475

ARTERIOVENOUS ANASTOMOSES IN SEAL SKIN. I1 255

level of the hair follicle and the deep dermis as the region extending from the sebaceous glands to the dermal-hypodermal junction.

RESULTS

1. Vasculature of the skin Tarasoff and Fisher ('70) described the gross

anatomy of the blood supply to the hind flipper of Callorhinus. Our observations were con- fined to the integument, which receives i ts blood supply from large arteries ascending tor- tuously through the hypodermal (blubber) layer and ramifying in the dermis. Considera- ble branching of arteries occurs at the level of the dermal-hypodermal junction, the junction of the reticular and papillary layers of the der- mis, and at a subepidermal level. AVAs com- monly arise from arteries at these levels.

2. Morphology of A VAs The AVAs were simple, coiled vessels con-

sisting of arterial, intermediate and venous segments (Vastarini-Cresi, '03). In Zalophus t h e coiling was more complex t h a n in Callorhinus.

3. Distribution and density of A VAs The distribution and density of AVAs in the

skin of the body and flippers of Zalophus and Callorhinus are listed in table 1. The distribu-

TABLE 2

Density of AVAs in the body and flipper skin of a subadult male sea lion Zalophus californianus and

a subadult male fur seal Callorhinus ursinus

Region Mean Sample size AVA density

Body skin Fore- and hind

flipper skin Foreflipper skin Hind flipper skin

Body skin Fore- and hind

flipper skin Fore flipper skin Hind flipper skin

2. californianus 4

8 4 4

C. ursinus 2

6 4 2

47.00k 11.54 ' 191.25+ 14.89 206.25k 25.35 176.75% 15.73

100.5 2 24.50 ' 951.50f 135.70 743.0 f 25.97

1,368.5 2 106.5 ~~~~~~~~ ~~~ ~

In bnthZ. californianus and C. ursinus the mean density of AVAs using Student's t test, was significantly greater in flipper skin than in body skin: P < 0.01.

In Z. californianus there was no significant difference between the mean AVA density of foreflipper and hind flipper skin: P =

0.05. In C. ursinus the mean density of AVAs in hind flipper skin was

significantly greater than in foreflipper skin: P < 0.01. ' Standard error of the mean.

Fig. 1 Ten arteriovenous anastomoses in the dermis of the foreflipper of Callorhinus ursinus, reconstructed free- hand from serial sections. Many AVAs arise from larger arteries in the skin, as illustrated here. Arteries stippled, veins black; arteriovenous anastomoses are numbered 1 to 10. (N.B. The scale is a guide only).

tion of AVAs in the different skin layers shows a marked difference between genera. In Zalophus the majority of AVAs (72%) occurred in the deeper layer of the dermis, whereas in Callorhinus most AVAs (76%) were found to be in the superficial layer of the dermis.

Table 2 shows the mean density of AVAs in body and flipper skin. InZalophus the density of AVAs was significantly greater, (P < 0.011, in the flipper than on the body, and there was no significant difference, (P = 0.05), in den- sity between the fore- and hind flippers. In Callorhinus the AVA density was significant- ly greater, (P < 0.01), in the skin of the flip- pers than tha t of the trunk, and significantly higher, (P < 0.011, in the hind flipper than the foreflipper. There was little difference in den- sity on the dorsal and palmar surfaces of the foreflipper. In both genera multiple sampling of skin from each region revealed a consid- erable variation in density (table 11, as has been observed in other species (Daniel and Pritchard, '56; Molyneux, '65). This variation can be explained by a grouping of AVAs around their arteries of origin (fig. 1).

DISCUSSION

In vivo studies of AVAs in the rabbit ear led Grant e t al. ('32) to propose tha t when body tempera ture rose, AVAs opened allowing large amounts of blood to flow rapidly through superficial veins where heat exchange could occur. Sherman ('63) by applying Poiseuille's

256 M. M. BRYDEN AND G. S. MOLYNEUX

equation, calculated t h a t blood flowing through an AVA whose diameter is approx- imately ten times greater than a capillary Le., 100 p compared to 10 p in diameter) would have a flow rate ten thousand times grea te r t h a n t h e capillary, per un i t of strength. Furthermore, based on normal capil- lary pressures, one millilitre of blood requires approximately six hours to flow through a cap- illary 10 p in diameter. An AVA with a diam- eter of 100 p would pass the same amount of blood in a fraction more than two seconds. In the sea lion, and to a much greater extent in the fur seal, blood flow through the flippers would increase enormously when all AVAs are open. Because there are large numbers of AVAs close to the bare skin surface of the flip- pers, this would result in very significant dis- sipation of body heat.

In bothZalophus and Callorhinus there were significantly greater numbers of AVAs in the skin of the flippers than of the body, which contrasts with the Weddell and elephant seals where no significant difference in AVA den- sity in skin from different regions of the body was observed (Molyneux and Bryden, '77). However, there were striking differences in the distribution and density of dermal AVAs between the California sea lion and the north- ern fur seal. These findings are consistent with the results of physiological and behav- ioural studies by other workers on these two genera, and lend strong support to the concept tha t AVAs occur in greater numbers in skin regions tha t are important in vascular ther- moregulation (Molyneux, '65).

California sea lions have a poor heat tol- erance in natural conditions (Whittow e t al., '71). I t has been shown tha t respiratory fre- quency does not increase during hyperthermia (Whittow e t al., '72), and tha t although active sweating occurs on the bare skin of the flip- pers, evaporative heat loss mechanisms are relatively ineffective (Matsuura and Whit- tow, '74). Arteriovenous anastomoses in the skin of the flippers possibly account for some loss of body heat while the sea lions are on land, but would be relatively ineffective in the warm climate in which these animals live, ex- cept possibly at night and on cool days. The density and distribution of AVAs in Zalophus are similar to those reported for a terrestrial mammal, the sheep (Molyneux, '65). However, the larger AVAs in the extremities of the sheep are possibly more effective in dissipa-

tion of body heat than the smaller anasto- moses in the flippers of the sea lion.

The density of AVAs in the skin of the Cali- fornia sea lion is considerably lower than in the Weddell seal, elephant seal or northern fur seal; in addition the majority of AVAs lie in the deeper layer of the dermis, and therefore further from the skin surface, in the sea lion than in those three species. Therefore i t seems unlikely tha t AVAs are important for regula- tion of body temperature in California sea lions on land, although they could account for significant dissipation of heat when sea lions a re in the water.

In comparison, northern fur seals when undisturbed can tolerate wide ranges of tem- perature on land (Bartholomew and Wilke, '56). However, as evaporative heat loss from the skin or the lungs would be minimal in the low temperatures and high humidity of the Pribilof Islands (Irving e t al., '62), it is ex- pected tha t vascular mechanisms would be important in controlling body temperature.

Northern fur seals are known to exhibit, on warm days, behavioural patterns on land tha t are believed to be thermoregulatory. Bartholomew and Wilke ('56) have described the spreading of the digits and fanning move- ments of the hind flippers which occur as the air becomes warmer than 13°C. Also Irving et al. ('62) showed tha t on land or in the water, the body skin temperature of Callorhinus was nearly constant, whereas the temperature of the flipper skin varied greatly. They con- cluded tha t the flippers were most important in the regulation of body heat dissipation, a concept which is strongly supported by our findings of a high density of AVAs located su- perficially in the skin of the flipper. Thus the highest density of AVAs found in the skin of the hind flippers can be related directly to the fanning movements and spreading of digits of the hind flippers in conditions of heat stress.

ACKNOWLEDGMENTS

This work was supported by a grant from the Australian Research Grants Committee. We are deeply indebted to Doctor R. Gentry for collecting and sending the fur seal skin samples to us. Thanks a re extended to Sea World, Queensland, for the sea lion material, and to L. Bell for technical assistance. D. Bailey, Department of Veterinary Anatomy, University of Queensland, kindly prepared the figure from our rough sketches.

ARTERIOVENOUS ANASTOMOSES I N SEAL SKIN. 11. 257

LITERATURE CITED

Bartholomew, G. A., and F. Wilke 1956 Body temperature in the northern fur seal, Callorhinus ursinns. J. Mammal., 37: 327-337.

Grant, R. T., E. F. Bland and P. D. Camp 1932 Observations on the vessels and nerves of the rabbit’s ear with special reference to the reaction to cold. Heart, 16: 69-82.

Irving, L., L. J. Peyton, C. H. Bahn and R. S. Peterson 1962 Regulation of temperature in fur seals. Physiol. Zool., 35: 275-284.

Matsuura, D. T., and G. C. Whittow 1974 Evaporative heat loss in the California sea lion and harbor seal. Comp. Biochem. Physiol., 48k 9-20.

Molyneux, G. S. 1965 Observations on the structure, dis- tribution, and significance of arterio-venous anastomoses in sheep skin. In: The Biology of the Skin and Hair Growth. A. G. Lyne and B. F. Short, eds. Angus and Robertson, Sydney, pp. 591-602.

Molyneux, G. S., and M. M. Bryden 1975 Arteriovenous an- astomoses in the skin of seals. I. The Weddell seal Lep- tonychotes weddelli and the elephant seal Mirounga leonina (Pinnipedia: Phocidae). Anat. Rec., 191: 239-252.

Peterson, R. S., and G. A. Bartholomew 1967 The natural history and behavior of the California sea lion. Am. SOC. Mamm., Special Publ. No. 1, pp. 1-79.

Ray, C., and M. S. R. Smith 1968 Thermoregulation of the pup and adult Weddell seal, Leptonychotes weddelli (Lesson) in Antarctica Zoologica, 53: 33-46.

Scheffer, V. B. 1964 Hair patterns in seals (Pinnipedia). J. Morph., 115: 291-304.

Sherman, J. L. 1963 Normal arteriovenous anastomoses. Medicine (Baltimore), 42: 247-267.

Tarasoff, F. J., and H. D. Fisher 1970 Anatomy of the hind flippers of two species of seals with reference to thermo- regulation. Can. J. Zool., 48: 821-829.

Vastarini-Cresi, G. 1903 Le anastomosi arterio-venose nell’uomo e nei mammiferi: studio anatomo-histologico. F. Sangiovanni, Napoli.

Whittow, G. C., D. T. Matsuura and Y. C. Lin 1972 Temper- ature regulation in the California sea lion fZalophus cali- fornianusl. Physiol. Zool., 45: 68-77.

Whittow, G . C., C. A. Ohata and D. T. Matsuura 1971 Be- havioural control of body temperature in the unre- strainedcalifornia sea lion. Comm. Behav. Biol., 6: 87-91.

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