Breathing Response to Thermal Stress

a. Species variation. As summarized in Table VI, the response varies according to species from a depression of breathing to extremely rapid open-mouthed panting. The t e r m panting should be reserved for situations in which there is not only an increased respiratory rate, b u t also a signifi­

cantly reduced tidal air volume (Hemingway, 1938). Small species, less t h a n 1 kg., in general do not increase their breathing, which is in agreement with their lack of other evaporative heat loss mechanisms. Marsupials of 1-10 kg.

in general show a two to three times increase of breathing under maximum tolerable stress, but panting occurs only in Didelphis. Marsupials depend more on evaporation of saliva for cooling. Panting is best developed in placentals 2 kg. or heavier; panting occurs at rates five t o twenty times t h e

TABLE VI BREATHING RESPONSE OF MAMMALS EXPOSED TO HEAT STRESS, TA ^ 40°°»B No change, or decrease 1.5-2.5 Times increase 3-4 Times increase Panting at rates indicated Dasyuridae Sminthopsis larapinta (0.01) Antechinus flavipes (0.05) Phascogale tapoatafa (0.1 l)c Sarcophilus harrisii (6.7) Phalangeridae Petaurus breviceps (0.12) P. norfolcensis (0.23) Trichosurus eburacensis (1.4) Didelphiidae Peramelidae Macropodidae Chiroptera Muridae Melomys littoralis (0.04) Hydromys chrysogaster (0.69) Uromys sherrini (0.51) Rattus conatus (0.09) Peromyscus sp. (0.03)1 Μ us musculus alb. (0.02)2 Rattus norvegicus alb. (0.2)2

S. crassicaudata (0.02) Dasycercus cristicauda (0.7) Satanellus hallucatus (0.65)C Schoinobates volans (1.1) T. spp. (2-5.1) Macrotis lagotis (0.86) Potorus tridactylus (1.0)C Setonyx brachyurus (3.9) ΨαΖΖα&ια spp. (2.8-19) Megaleia rufa (30.7) Macropus major (30.8) Pteropus poliocephalus (0.21) Myotis spp.16 Macrotus californicus15

Isoodon obesulus (1.2) Wallabia elegans (8.8)

Didelphis marsupialisu (4) 5 X ik/us musculus alb. (0.02)3 Rattus norvegicus alb. (0 2)3

98 /tofcerf Af. Cfeew

Miscellaneous placental mammals Donkey (97)4 Camelus dromedarius (240)6 Macaea mulatto (1.6) Rabbit (2) 8X6 Cat (4) 4.5 X7 Dog (14) 12-20 X*·11 Berkshire pig (54) 7 X9 Merino sheep (30) 12X10 European breeds, cows 7-8 X12 Indian breeds, cows 5-6 X12 Goat (25) 13 X13 α Weights in kilograms given in parentheses. 6 Superscript numbers indicate sources: 1. Chew (1951), 2. Adolph (1947a), 3. Lee (1950), 4. Adolph and Dill (1938), 5. K. Schmidt- Nielsen et al. (1957), 6. Lee et al. (1941), 7. Robinson and Lee (1941a), 8. Robinson and Lee (1941b), 9. Robinson and Lee (1941c), 10. Lee and Robinson (1941), 11. Flinn (1925), 12. Kibler and Brody (1950a, 1951), 13. Andersson et al (1956), 14. Higginbotham and Koon (1955), 15. Reeder and Cowles (1951). All unnumbered species. Robinson and Morrison (1957). c Change to open-mouth breathing during stress, but have no more than slight increase in rate

100 Robert Μ. Chew basal breathing rate. Among the larger mammals t h a t show no breathing response when heated, the Tasmanian devil, Sarcophilus harrisii, apparently sweats very effectively and the camel sweats and stores heat.

6. Mechanics of panting. Hemingway (1938) has analyzed the breathing of dogs heated by diathermy. I n the prepanting stage there is a gradual three- to fourfold increase in rate of breathing without reduction in tidal volume; with panting there is a further two- to threefold increase in rate, but with a 2 5 - 3 5 % reduction in tidal volume. A t intervals during panting the rate and tidal volume return to prepanting levels.

The most economical breathing rates can be calculated from measure­

ments of the resistance, compliance, and inertance of the respiratory systems of anesthetized animals. Crosfill and Widdicombe (1961) found t h a t the calculated values correspond closely to the observed rates in a variety of species. T h e work required per unit of ventilation is least at the natural resonating frequency of the system, when the effects of the compliance and inertance of the system cancel each other, and the volume flow of air is exactly in phase with the driving force of muscular contraction and elastic recoil (Hull and Long, 1961; Crawford, 1962). Crawford (1962) found t h a t the panting frequency of 12-kg. dogs is 5.33 cycles per second, as compared with an estimated natural resonance of their respiratory systems of 5.28 cycles per second. The high natural frequency of cats, 11.5 cycles per second (Brody et al., 1959) m a y prohibit effective panting in this species. The natural frequency for humans, 5.8 cycles per second (DuBois et al., 1956) m a y be prohibitive in a 70-kg. mammal, although other factors are also involved in limiting the ability to pant.

Panting provdies a maximum of evaporation with a minimum of alveolar gas exchange. As the tidal volume is decreased, a greater percentage of each breath contacts only the moist surfaces of the dead-air space (which accomplish most of the humidifying of the inspired air) and less enters the alveoli. Only air coming into the alveoli can cause a "flushing out of CO2" and upset acid-base balance. Alveolar flushing can be lowered by reducing tidal air volume and by increasing the volume of air in the lungs, both of which occur in dogs (Hemingway, 1938). As panting begins, the lungs are expanded by means of the abdominal muscles and maintained so during thoracic panting movements. I n spite of these adjustments the dog m a y reduce its blood alkali reserve by about 5 0 % in 4 hours at 50°

(Flinn, 1925).

I n some mammals only closed-mouthed panting occurs, b u t others characteristically change to open-mouthed panting when stress exceeds a certain point. According to Scott (1954) mouth breathing is hampered in most mammals because the normal position of the epiglottis is above the soft palate; only in anthropoids does the larynx opea. into the oropharynx.

TABLE VII RESPIRATORY WATER LOSSES OF PANTING MAMMALS Animal0** B0 TA R.H. Respiratory I.W.R Cal./min. % Heat ventilation production (kg.) (°C.) (%) (l./min.) (gm./min.) Brown Swiss cow (d)1 493 41 60 300 5.49 3.18 29.5 Jersey cow (d)1 367 41 60 210 3.84 2.22 31.5 Brahman cow (d)1 465 41 60 147 2.69 1.56 22.6 Brahman cow (l)1 358 41 60 138 2.53 1.47 22.8 Rabbit2 3.5°" 41 32 1.7 0.059 0.034 19c Cat3 3.5°" 41 32 0.86 0.029 0.017 9.4C Dog4 16° 41 32 9.8 0.326 0.189 57e Sheep8 27* 41 32 9.5 0.316 0.183 29c Pig6 59d 41 32 10.1 0.336 0.195 21« Dog7 — 46 20 — 4.13 — — Karakul sheep8 — — — — 1.67 — — β Superscript numbers indicate sources: 1. Kibler and Brody (1950a, 1952), 2. Lee et al. (1941), 3. Robinson and Lee (1941a), 4. Robinson and Lee (1941b), 5. Lee and Robinson (1941), 6. Robinson and Lee (1941c), 7. Kanter (1954), 8. Paducheva et al. (1957). b (d) = dry, (1) = lactating. • Assuming heat production as 130% of basal metabolic rate as read from Fig. 13.7 in Brody (1945). d Assumed as a reasonable weight.

102 Robert Μ. Chew c. Physiological mechanisms controlling breathing. Breathing during heat stress is controlled by centers in the hypothalamus. A very discrete " h e a t loss center" has been demonstrated in t h e goat, electrical stimulation of which causes vigorous panting (Andersson et al., 1956). Panting can be evoked in the cat by heating of the hypothalamus (Strom, 1950). When heat stress is exogenous rather t h a n metabolic, T^s is more influential in causing panting t h a n T^r, in sheep (Macfarlane et al., 1958a) and cattle (Gaalaas, 1945). I n Welsh mountain sheep, and in calves, panting m a y begin before any rise in T^r or in temperature of the blood circulating to the brain (Bligh, 1957b, 1959). In these sheep, stimulation of receptors in both the nasobuccal mucosa and skin was necessary for maximal normal panting response, though the skin receptors were more influential. Warming of t h e calves' nasobuccal surfaces was but a feeble stimulus to panting (Bligh, 1957a).

However, breathing rate is usually analyzed in terms of T^r. The critical T^r at which panting begins is: white mouse 41.1°, white rat 40.6°, rabbit 40.0°, pig 39.2°, cat 39.4°, dog 37.8°, sheep 40.6° (Lee, 1950). European breeds of cows begin to p a n t at 38.238.4°, and Indian breeds p a n t at 3 8 . 7 -38.8° (Kibler and Brody, 1950b, 1952). The rate of breathing of cows is not significantly correlated with T^r, b u t respiratory volume often shows a high positive correlation (McDowell et al, 1953a).

d. Effectiveness of panting. Estimates of I . W .r for panting m a m m a l s are given in Table V I I . The dog is most effective at panting, losing most of its heat in this fashion ( ^ 5 7 % ) . Most panting mammals eliminate 2 0 - 3 0 % of their heat production by I.W.^r, but the cat is much less effective and supplements its evaporation by licking itself with saliva.

I n Merino lambs I.W.^S and I.W.^r are approximately the same at air temperatures below thermoneutrality. Above 30° both increase rapidly, but respiratory loss more so, until at 45° it is 6 8 % of total evaporation;

I.W.^r also has a greater functional reserve. At 43°, when cutaneous evapo­

ration is blocked, the lambs can increase their respiratory evaporation a t least 4 3 % ; however, when I . W .^r is blocked, there is no significant com­

pensatory increase in I.W.^S (Alexander and Williams, 1962).

2. Salivation in Response to Heat Stress

a. Nature and taxonomic distribution of salivation. Licking of saliva, as a regulatory process, is best developed in marsupials. Of the Australian species studied by Robinson (1954) and Robinson and Morrison (1957), 22 out of 27 showed some response, and it occurs also in Didelphis marsupialis (Higginbotham and Koon, 1955). N o t only is the reflex of copious salivation involved, but also a behavior p a t t e r n to spread this saliva methodically

onto the fur, where it can be effective in dissipating body heat. I n the smaller marsupials licking is usually limited to the paws and base of tail, whereas the macropods profusely lick their limbs, abdomen, and tail I n marsupials salivation and licking begin after only a small rise in body temperature, at T^r 38° in Didelphis and 39° in Setonyx (Bartholomew, 1956), but in most placental mammals salivation does not begin until at least T^r 40-41°. Among placentals, salivation has been reported for: Peromyscus (Sealander, 1953; Murie, 1961) Dipodomys (the Schmidt-Nielsens, 1952);

mouse, rat, guinea pig (Herrington, 1940; Stigler, 1930); Citellus harrisi (Chew, 1958); C. leueurus (Hudson, 1962); Neotoma lepida (Lee, 1963);

cat and pig (Robinson and Lee, 1941 a,c); rabbit (Keeton, 1924; Lee et al., 1941); cattle (Robinson and Klemm, 1953); fruit bat, Pteropus polioce-phalus; and t h e giant naked-tailed rat, Uromys sherrini (Robinson and Morrison, 1957). Of these only the cat thoroughly licks itself, covering all available parts of the body to the point where they drip. I n the rabbit, cattle, and pig the saliva simply drools onto the ground. Nasal secretions of the pig keep the snout moist and m a y slightly increase I.W.^r.

Peromyscus eremicus, a species which probably has evolved in arid habitats, resorts to saliva-spreading much less readily t h a n P. maniculatus, a mesic-habitat species. Perhaps the more lavish use of water by the latter species is correlated with its evolutionary history of infrequent experience of high temperatures in its natural habitat, along with the availability of water to replace salivary losses, while in P . eremicus water conservation has taken precedence over thermoregulation (Murie, 1961).

A similar "reluctance" to dissipate water for heat regulation is seen in t h e comparison of desert bandicoots with those from more mesic habitats (Morrison, 1962).

b. Effectiveness of salivation. T h e licking of saliva would appear to be a very effective means of regulating body temperature in marsupials. When Didelphis are anesthetized, and consequently cannot lick themselves, they die at T^a of 43° in spite of rapid panting; conscious individuals regulate successfully (Higginbotham and Koon, 1955). Bartholomew (1956) showed t h a t Setonyx brachyurus has no difficulty in maintaining a T^r of about 39°

when T^a is 44°, and he attributes this to cooling by evaporation of saliva.

However, Bentley (1960) found t h a t after 3 hours at T^a of 40°, the rectal temperatures of normal, licking animals were not significantly different from those of animals prevented from licking. Further, the arms and feet of Setonyx were wet even when licking was prevented. These d a t a suggest t h a t I.W. and sweating are of primary importance in thermoregulation, and t h a t more experiments are needed to determine t h e significance of saliva licking.

104 Robert Μ. Chew I n Dipodomys, the wetting of the throat and chest with saliva tempo­

rarily reduces body temperature below T^a (the Schmidt-Nielsens, 1952).

However, in kangaroo rats and other small placentals, salivation is probably only an extreme emergency mechanism, or simply the result of overheating of brain centers.

c. Negative effects. Drooling of saliva onto the ground is a drain on water balance without any benefit. I n cattle, drooling occurs at rates up to 1.5 liters per hour (Robinson and Klemm, 1953) and 9.5-15 liters per day (Bonsma, 1940). This is not only an important water loss, b u t 15 liters per day involves a salt loss of about 8 gm. which complicates recovery from dehydration. Robinson and Lee (1941c) found t h a t their pigs drooled at rates u p t o 0.5 liters per hour or 1.3% B⁰ per hour.

3. Sweating

a. General description and species occurrence. The emphasis t h a t has been placed on the study of sweating in m a n (see review, Randall, 1953; Weiner and Hellmann, 1960) has probably prejudiced work on other mammals, and the failure to observe in mammals the copious response typical of humans has led to persistent erroneous conclusions t h a t sweating is absent.

In a fair number of mammals, apocrine glands are generally distributed over the skin in association with hair follicles; eccrine glands are present on the plantar surfaces of m a n y species. But, eccrine glands are distributed over the general surface only in m a n and other primates. I t is the apocrine glands t h a t are potentially capable of contributing t o thermoregulation.

Plantar eccrine glands can dissipate little heat, b u t their sweat m a y be important in keeping t h e thick corneum of t h e pads flexible and in improving traction with t h e ground.

Findlay and Yang (1950) and Hafez et al. (1955) describe the apocrine glands of Bos. Secretory cycles of short duration can be recognized in histological preparations; seasonal changes in t h e volume of t h e glands also occur (Hayman and N a y , 1958). Takagi and Tagawa (1959) give a cyto-logical and cytochemical study of horse sweat glands, and Ring and Randall (1947) describe the eccrine glands of the rat plantar tubercles.

I n cattle all hair follicles have associated apocrine glands, and hairs can be used as an index of the number and distribution of glands. I n Bos spp.

the ratio of sweat glands per square centimeter is about 1:10:20 in B.

bubalis, B. taurus, and B. indicus, respectively, b u t the glands of B. bubalis are three times as large as those of B. taurus (Yamane and Ono, 1936;

Findlay and Yang, 1950; Dowling, 1955; Hafez et al., 1955). There is con­

siderable variation in the shape, size, and density of glands in different breeds of cattle (Nay, 1959). Sindhi and Sahiwal cattle (Bos indicus) are

very unusual in t h a t their sweat glands are so large t h a t , at normal den­

sities of 1200-1500 glands per square centimeter, the glands touch and form a "continuous" layer of fluid in the skin about 1 m m . thick and 750 μ below the surface of the skin. This layer can store about 480 ml. of sweat per square meter of skin surface, in comparison to 80 ml. stored in European breeds of cattle.

I n dog breeds, glands are more numerous in the poodle and pinscher t h a n in t h e sheep dog and fox terrier (Claushen, 1933). I n comparing breeds it is necessary t o recognize t h a t t h e density of glands decreases with growth and increasing nutritional plane. I n sheep, and probably cattle, the total number of follicles is present a t or shortly after birth, and as surface area increases, gland density decreases. I n t h e buffalo, density changes from 10,560 per square centimeter in 5-month embryo, to 1248 per square centi­

meter in newborn calf to 400 per square centimeter in 3-year-old adult (Hafez et al., 1955). I n full-grown shorthorn cattle, density m a y vary from 764 per square centimeter in a high-fed animal to 1064 in a low-fed one (Dowling, 1955). T h e density of glands also varies regionally in cattle (Findlay and Yang, 1950) and dogs (Claushen, 1933).

Apocrine glands are associated with t h e hair follicles of the general body surface in t h e platypus (Ornithorhynchus anatinus), and these glands are more specialized t h a n those of some primates (Montagna and Ellis, 1960a).

Apocrine glands have been histologically identified in quite a few different marsupials (Hardy, 1947; Green, 1961). Sweat glands are present, and usually large in size, in amphibious mammals, such as Chironectes, Neomys, Galemys, Desmana, Lutra, Mustela, Castor, Ondatra; sweat glands are also well developed in pinnipeds, e.g., Callorhinus, Eumetopias, Odobenus, and Phoca (Sokolov, 1962a; M o n t a g n a and Harrison, 1957). However, there are no skin glands in cetaceans.

Apocrine glands have been described in Sorex and Blarina (Johansen, 1914; Eadie, 1938), the horse (Evans et al., 1957), camel (Dowling and N a y , 1962; Lee and Schmidt-Nielsen, 1962), sheep (Dowling, 1955), bear (Krumbiegel, 1954), goat, pig, and rabbit (Scheunert and T r a u t m a n n , 1951).

I n Spermophilopsis, Rhombomys, Meriones, Citellus, and Sciurus, sweat glands were found only in the soles of the paws (Sokolov, 1962b). Sweat glands are absent in the skin of Jaculus jaculus (Riad, 1960b).

M o n t a g n a and associates have studied the sweat glands of a variety of primates (Montagna and Ellis, 1959, 1960b; M o n t a g n a et al., 1961a;

Yasuda et al, 1961; Ellis and Montagna, 1962; M o n t a g n a and Yun, 1962a-c; Parakkal et al, 1962). While specialized eccrine and apocrine glands are morphologically and histochemically distinct in t h e Pongidae, in prosimians there is either only one t y p e of gland, with both eccrine and apocrine

106 Robert Μ. Chew characteristics (as in Nycticebus coucang) or there are apocrine-like glands on the body surface, in association with hair groups, and eccrine-like glands on the plantar and palmar surfaces. The absence of clear differentiation of glands in primitive prosimians suggests t h a t eccrine and apocrine types have differentiated from a common ancestral gland type. In the prosimians studied, the apocrine glands are probably functional in heat regulation except in Galago, where they seem to be important only as scent glands. In G. crassicaudata "sweat" glands are quite sparse. I n all the prosimians t h a t have been examined, the very thin skin is poorly vascularized and m a y not have an active role in heat loss by radiation and conduction. I n the Pongi-dae, Hylobates, Pan, and Gorilla all have both apocrine and eccrine glands in the general body surface; both presumably function in temperature regulation. I n Hylobates the apocrine glands are more numerous. In Gorilla the eccrine glands are largest and most numerous in the glabrous skin areas, while apocrine glands are more characteristic of the hairy areas. The baboon (Papio doguera) is unusual in t h a t it has more eccrine t h a n apocrine glands. I n simians generally there is a concentration of apocrine glands in the anterior part of the chest; the axillary glands typical of Pongidae m a y be derived from these.

b. Functioning of sweat glands. Information on the functional status of sweat glands is scant, in spite of t h e easy methods of verification of oc­

currence of sweating. When sweating is sufficiently copious it m a y be grossly observed, otherwise sweating from individual pores can be seen with a microscope or active pores can be chemically visualized by various methods: bromothymol blue and sodium carbonate (Ferguson and Dow-ling, 1955), alcoholic ferric chloride (Silverman and Powell, 1944), iodine starch (Wada and Takagaki, 1948).

Except for the horse, donkey, cattle, and camel, sweating has not been directly observed to occur regularly in response to heat stress. Aoki (1955) reviews the literature on observations on the dog. Spontaneous sweating can sometimes be observed in restricted areas of violently struggling dogs and m a y occur normally in the Skye terrier and hairless Chihuahua.

Aoki and W a d a (1951) showed t h a t the apocrine glands of dogs will respond to radiant heating sufficient to raise T⁸ to approximately 38.6°, b u t they found sweating only in the irradiated areas, in spite of considerable rise in T^r. They proposed t h a t this sweating is principally for protection against heat damage to the skin. They found little evidence for nervous control of sweating; the apocrine glands responded locally to injections of epinephrine and acetylcholine, and the sweating seen occasionally in struggling dogs m a y be an epinephrine response. I n contrast, Lemaire et al. (1958) found sweating on both sides of dogs heated only on one side ( T^r 40°, T⁸ 43° on

heated side, 38° on protected side), and sweating on thorax and abdomen in dogs breathing hot air (Τ^Γ 40-41°, T⁸ 32-33°). F r o m this they inferred t h a t sweating in dogs is dependent on central mechanisms, as in man.

Sweating in t h e horse is normally under humoral control. When horses are exercised in the sun, their plasma epinephrine increases to 3 Mg. per liter; injections of epinephrine in amounts of 1-7 μg. per kilogram B0

induce sweating for 10-15 minutes in resting horses (Evans et al., 1956).

1956). Acetylcholine also produces sweating, probably by causing vasodi­

lation a n d / o r release of epinephrine. Stimulation of the sympathetics inhibits sweating, probably by local vasoconstriction; section of the cervical sympathetics is followed by spontaneous sweating in the denerva-ted area (Bell and Evans, 1956). Enforced activity in the tropics m a y result in loss of sensitivity of the glands to epinephrine and in failure of sweating (Evans et al., 1957).

I n the slow loris (Nycticebus coucang) the primitive apocrine glands on the body surface respond to small injections of epinephrine with a copious, fetid secretion; there is no response to acetylcholine although the glands are surrounded by nerve cells which contain cholinesterase (Montagna et al., 1961a). I n Lemur catta, both the sweat glands on the soles and palms, and those on the general body surface, secrete in response to epinephrine

(Montagna et al, 1961b).

Sweating has been observed in Bos bubalis (Badreldin and Ghany, 1952), and B. indicus (Barrison-Villares and Berthet, 1952; Robinson and Klemm, 1953), b u t its physiological control has not been investigated. I n Holstein X Syrian cattle, the rate of evaporation from t h e skin is greatest (in order) on the muzzle, lateral neck, ventral neck, and front flank, and least on abdomen, forehead, and udder. Regional differences are highly significant and generally follow the regional differences in distribution of sweat glands.

There was no correlation between r a t e of evaporation and weight or density of fur (Berman, 1957). I n American B r a h m a n calves, sweating apparently is under humoral control, being adrenergic rather t h a n cholinergic (Taneja, 1956).

For Elephas maximus Benedict (1936) reports one instance of intense sweating after the animals had eaten something upsetting, b u t histologic studies of K u n o (1956) and Smith (1890) showed no sweat glands, and F r a d e (1954) reports sweat glands in only certain "rare spots" on t h e body.

I n t h e white rhinoceros (Ceratotherium simum), very large apocrine glands are found coiled around t h e bases of t h e hair follicles (Cave and Allbrook, 1959), and this animal sweats freely when it is persistently dis­

turbed in the daytime and kept out in the sun.

108 Robert Μ. Chew Tubulo-acinar glands are distributed over t h e entire body surface of the little brown b a t (Myotis lucifugus), including the flight membranes, and are particularly found clustered around the tactile hairs of the snout (Sisk, 1957). Local electrical stimulation and pilocarpine injections cause small watery drops to appear around the tactile hairs, but no response was observed during heating of the animals under a light bulb. These glands show a seasonal increase in size in late summer and in the early p a r t of the hibernation period, which m a y be attributable to an accumulation of unused secretion.

I n several other mammals there is indirect evidence of sweating. The Tasmanian devil has excellent heat tolerance in the absence of panting or salivation, and apparently sweats (Robinson and Morrison, 1957). Riek et al. (1950) assume t h a t sweating occurs in sheep, since the observed vaporization cannot be accounted for by I.W. I n t h e cebus and macaque monkeys and the dog, the occurrence of skin temperatures several degrees below rectal at T^a of 42° also indicates sweating (Hardy, 1955; Robinson and Morrison, 1957).

c. Effectiveness of sweating. Sweating is much more effective t h a n I.W.^S in cooling t h e skin, since it produces a maximum V P^e and percentage of

c. Effectiveness of sweating. Sweating is much more effective t h a n I.W.^S in cooling t h e skin, since it produces a maximum V P^e and percentage of

In document Water Metabolism of Mammals (Pldal 55-73)