comparative aspects of the metabolism and thermal biology of elephant-shrews (macroscelidea)

Mammal Rev. 1995, Volume 25, Nos 1 and 2, 61-78. Printed in Great Britain.

Comparative aspects of the metabolism and thermal biology of elephant-shrews (Macroscelidea)

M.R. PERRIN Department of Zoology and Entomology, University of Natal, PO Box 375, Pietermaritzburg, Natal, South Africa

ABSTRACT The metabolic rates of elephant-shrews are typical of eutherian mammals and follow allometric relationships. They do not exhibit ‘primitive’ characteristics in relation to thermal biology as shown by other insectivores, and their reduced metabolic rates are interpreted as adaptive responses to habitat variables. Stable body temperatures are maintained over a wide range of environmental extremes. Hyperthermia is prevented by evaporative water loss and peripheral vasodilation, whereas hypothermia is probably more widespread than current data suggest. Elephantulus rozeti fiom the Atlas Mountains of North Africa has been shown to exhibit spon- taneous daily torpor. Although the metabolic rates of macroscelids approximate those of tupaiids, they differ in maintaining a high stable body temperature below the thermoneutral zone.

The ecophysiology of the species comprising the three genera studied are different. Petrodromus (tetradactylus) maintains a relatively low body temperature and metabolic rate, but has the lowest relative evaporative water loss and the highest absolute thermal conductance. These characteristics are correlated with a thermally stable but warm, humid environment, and are not explained by taxonomy. The thermal biology and metabolism of species of the other two genera, Macroscelides and Elephanfulus, are interpreted as adaptations to thermally variable, arid environments. Although physiologically well adapted, the thermal and metabolic strategy of Macroscelides @roboscideus) is greatly influenced by its nocturnal behaviour and use of a burrow. The body temperatures and metabolic rates of Elephantulus species are markedly similar, and evaporative water loss varies with water availability in their respective habitats. Species differences are discussed in relation to habitat, behaviour and taxonomy.

It is suggested that the common metabolic characteristics of elephant-shrews were evolved in a stem ancestor, whereas adaptive characters include physiological and behavioural responses to control evaporative water loss and thermal conductance. The metabolic strategy of elephant- shrews contributes to their ecological and evolutionary success.

INTRODUCTION Considerable controversy exists over the taxonomic status of elephant-shrews (Corbet, 1955, 1966; Corbet & Hanks, 1968; Butler, 1995) but like other insectivorous small mammals they are considered morphologically primitive (Dawson, 1973). The elephant-shrews were formerly classi- fied as a family (Macroscelidae) of the order Insectivora, but they are now recognized to be sufficiently distinct from all other insectivores to constitute the separate order Macroscelidea (Butler, 1956; Patterson, 1965; Butler, 1972). Unlike the insectivorans they have enlarged brains, acute vision, specialized dentition (Patterson, 1965; Butler, 1995), hindgut fermentation (Woodall, 1987; Woodall & Mackie, 1987) and a unique locomotory habit (Vaughan, 1972). Elephant-shrews inhabit either arid zone ecosystems, in which case they are small-bodied, or tropical deciduous forest, where they are large-bodied. They are primarily insectivorous, invariably specialists on ants or termites (McNab, 1984), yet have the capability of utilizing plant foods. This,

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62 M. R. Perrin

however, is a seasonal phenomenon (Kerley, 1992,1994). Their social organization is based on monogamy and territoriality (Rathbun, 1979; FitzGibbon, 1994).

The order Macroscelidea comprises two families, the Rhynchocyonidae and the Macroscelidae. Three distinctive large-bodied, tropical forest species represent the genus Rhynchocyon and comprise the family Rhychocyonidae. The family Macroscelidae comprises three genera, Petrodromus (one species), Macroscelides (one species) and Elephantulus (10 species) (Corbet & Hanks, 1968; Corbet, 1995). While the Round-eared Elephant-Shrew Macroscelides proboscideus is confined to southern Namibia and the south-western Cape of South Afirica (Skinner & Smithers, 1990), the Four-toed Elephant-Shrew Pefrodromus fetrahctylus is predominantly a tropical species whose distribution extends southwards to the Mocambique plain (Rathbun, 1979). The differences in diurnal and seasonal climatic extremes encountered by species from different habitats and latitudes must be very considerable although no quantitative data exist. The genus Elephanfulus, unlike the previously mentioned monospecific genera, comprises a range of species, distributed from North Africa to the Cape (Corbet & Hanks, 1968). While Macroscelides aid Elephantulus species are arid zone specialists, occurring in areas where rainfall averages 300mm or less per annum, P. terradactylus, like the three species of the genus Rhynchocyon, is a forest species that encounters relative thermal constancy and high relative humidities.

Little is known of the physiology of elephant-shrews. Most attention has been given to reproductive biology (Neal, 1995). owing to their characteristic but unusual form of ovulation (van der Horst, 1964; Tnpp, 1971), the reproductive peculiarities of the male (Woodall, 1995), distinct K-selection (Neal, 1994), and monogamy (Rathbun, 1979; FitzGibbon, 1994). Some attention has also been given to ascertaining the degree of berbivory in terms of fibre fermentation and associated digestive processes (Woodall & Mackie, 1987; Woodall, 1987; Spinks & Perrin, 1995). Aspects of environmental physiology studied include the thermal biology and water turnover rates of afew small-bodied, arid zone Elephantufus species (Leon, Shkolnik & Shkolnik, 1983; McNab, 1984; Roxburgh & Perrin, 1994; Du Toit, Perrin & Fourie, in press).

The primary purpose ofthis review is to compare aspects ofthe thermal biology ofthree species of elephant-shrew that occupy different environments, and belong to different genera. They are the Round-eared Elephant-Shrew M. proboscideus, the Rock Elephant-Shrew Elephantulus myuw, and the Four-toed Elephant-Shrew P. fetrudactylus. The second aim is to review the thermal biology of several species belonging to the genus Elephantulus. Comparative data are presented on the Short-snouted Elephant-Shrew E. brachyrhynchus and the Bushveld Elephant-Shrew E. infufi (C.T. Downs & M.R. Pemn, unpublished data). These are interpreted in relation to published results on the Cape rock Elephant-Shrew E. edwardii from the Western Cape of South Africa (Leon ef al. 1983), the Rufous Elephant-Shrew E. nrfescens of East Africa (McNab, 1984), and Rozeti’s Elephant-Shrew E. rozeti of North Africa (Seguignes, 1983).

The specific objectives of the study were (i) to review the basal metabolic rate (BMR) of each species of elephant-shrew in relation to a range of ambient temperatures (T,), to enable comparison with predicted (allometric) values for insectivores and eutherians; (ii) to compare the zones of thermal neutrality (TNZ) and thermal preference of individual species, and where possible, to correlate them with aspects of the thermal environment, and (iiii) to contrast species-specific capacities to regulate body temperature above and below the TNZ in relation to their thermal conductance (C,), evaporative water loss (EWL) and heat production (HP). A summary of some ofthe terms and con- cepts used in discussing metabolism and thermal biology is given in Appendix 1.

One can hypothesise that because BMR is mass-specific, the relative, but not the absolute, BMRs of small-bodied elephant-shrew species will be higher than those of large-bodied species. However, because the macroscelids are not phylogenetically related to insectivorans, the low

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Thermal biology of elephant shrews 63

metabolic rates and thermolability characteristics of that taxon (Leon et al., 1983; Roxburgh & Perrin, 1994) should not be anticipated. The arid zone or xerophilic species of elephant-shrews might be expected to exhibit reduced BMRs as an adaptation to resource scarcity (Downs & Perrin, 1990), and myrmecophagous (ant-eating) (McNab 1984) and herbivorous feeding habits (Woodall & Mackie, 1987; Woodall, 1987; Spinks & Perrin, 1995). K-selection is another correlate of reduced metabolism in small mammals (Pemn, 1980; Neal, 1994), and a characteristic of the reproductive biology of elephant-shrews that warrants further investigation (Neal, 1995).

Subject species P. tetraciactylus (body mass 206 g; Table 1) is distributed in central and east Africa but its geo- graphical range extends to southern Africa along the Mocambique Plain. The presence of the Four-toed Elephant-Shrew is discontinuous, however, because it is associated with the availability of forest or woodland with dense underbush (Skinner & Smithers, 1990). It is generally absent from areas with a mean annual rainfall of less than 700 mm. The species is diurnal, terrestrial and uses hollow logs, termite mounds or dense bush for cover.

M. pruboscideus (body mass 39 g; Table 1) is confined in its distribution to the South West Arid Zone of the African continent. Round-eared Elephant-Shrews occupy open country with a shrub bush or sparse cover, on hard gravel plains or loose sandy soils, and are known to occupy burrows (Skinner & Smithers, 1990).

E. intufi (body mass 47 g; Table l), the Bushveld Elephant-Shrew, occurs in the south-west of southern Africa, in areas with less than 200 mm rainfall per annum and generally devoid of surface water (Skinner & Smithers, 1990). Scattered low bush cover is an essential habitat requirement.

E. brachyrhynchus (body mass 45 g; Table l), the Short-snouted Elephant-Shrew, is widely distributed in Africa (2ON-26OS) with the exception of the Sahara and the west-central rain forest zones. For elephant-shrews it occurs in relatively mesic grasslands, with scrub bush or scattered trees for cover (Smithers & Skinner, 1990).

E. ehvardii (body mass 50 g; Table I), the Cape Elephant-Shrew, inhabits Fynbos vegetation in the Mediterranean climatic zone ofthe Cape Province of South Africa Rocky areas with fissures and crevices provide refugia from predators and unfavourable climatic conditions. The animals experience semi-arid conditions for approximately 6 months of the year during hot dry summers, when solar radiation is intense and there is an absence of surface water. Winters, however, can be wet and cold with the occasional occurrence of snow (Leon et al., 1983).

E. myurus (body mass 65 g; Table l), the Eastern Rock Elephant-Shrew, frequents rocky outcrops on hilly terrain in the central upland plateau grasslands of South Africa (Du Toit, 1993). Semi-arid conditions are experienced for 8 months of the year, with intense solar radiation and high temperatures (35-40 "C) in summer, and an absence ofperennial surface water, accompanied by subzero temperatures, in winter. Neither nests nor burrows are constructed and the Eastern Rock Elephant-Shrew takes cover in rocky outcrops.

E. mfescens, the Rufous Elephant-Shrew, occupies the dry woodland and steppe zones of East Africa (Corbet & Hanks, 1968).

E. ruzeti, the North African Elephant-Shrew, ranges through the Mediterranean and subdesert zones of north-western Africa and from sea-level to 11 10 m in the Atlas Mountains (Corbet & Hanks, 1968). It therefore experiences a typical coastal mediterranean climate, semi-desert conditions, and a montane environment.

Thermal parameters The effects of ambient temperature (T,) on body temperature (T,), oxygen consumption (VO,), evaporative water loss (EWL) and thermal conductance (C,) of adult subjects have been deter-

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mined (Seguignes, 1983; Leon et al., 1983; McNab, 1984; Roxburgh & Perrin, 1994; Du Toit, Perrin & Fourie, 1995; C.T. Downs & M.R. Perrin, unpublished data). Generally, individual subjects were weighed and equilibrated for several hours prior to the experimental temperature in a controlled environment room or chamber (Ta f 1 "C; dry air), however, at extreme Ta (5 "C and 40 "C), equilibration periods were reduced to about 1 h to reduce stress. Experimentation was carried out during the day when elephant-shrews were inactive, non-fasting and post-absorptive.

Thermocouples connected to digital display thermometers were used to measure the ambient temperature in the respirometer chamber and the rectal temperatures of the elephant-shrews. VO, and EWL were measured simultaneously at each temperature using open-circuit airflow systems (Depocas & Hart, 1957). Air was dried over silica-gel before flowing into a respirometer chamber and again before entering an oxygen analyser. Flow rates were controlled and measured using a flowmeter. Carbon dioxide was removed from the air using a column of soda lime before entering the 0, analyser. Data loggers or chart records were used to continuously record VO,,

Standard runs were used to determine average per cent oxygen influx into the respirometer for about 60 min, before each subject was placed in the chamber. Mean percentage of oxygen consumed was used to calculate efflux rates. Influx and efflux rates were corrected to STP, and used to calculate VO, [typically using the equations of Hill (197211. Mass increase of the silica-gel column drying excurrent air was used to calculate the EWL of

each subject while in the chamber. Measurements were discarded if animals urinated in the respirometer chamber.

Dry thermal conductance (Cd), the rate of dry heat transfer per unit area to/or from an animal per OC temperature difference between the animal (T,) and its environment (7'J excluding heat lost through EWL, was calculated from oxygen consumption and temperature data (Dawson & Schmidt-Nielsen, 1966).

At T8 below the TNZ, the rate ofmetabolism of a homeotherm is proportional to the temperature differential between its body and the environment. Minimal thermal conductance (Cmin), including EWL, measures ease of heat loss when the metabolic rate approximates resting metabolism, and was also calculated using a general formula (Scholander et al., 1950).

DISCUSSION

Comparative aspects (Table 1)

Body temperature Over a wide range of environmental temperatures (Ta = 5-38 "C), elephant-shrews maintain body temperature within a narrow range (T, = 34-39 "C: mean approximates 37 "C). At low Ta, T, tended to be slightly depressed and variation occurred between species (Fig. I). At Ta = 35 "C, equivalent to thermoneutrality in most species, T, lay within the range 37-39 "C. While the Tb of M. proboscideus approximated that of the Elephantulus species, the Tb of P. tetrahctylus was generally 1-2 "C lower. Above the TNZ, T, increased rapidly in all species examined, except P. tetradactylus. E edwardii and E myurus maintained T, within more precise limits, except above the TNZ, than did the other Elephuntulus species. The greatest difference in Tb profiles occurred between the genus Petrodromus (P. tetradactylus) and the other two genera (Macroscelides and Elephantulus) which are collectively referred to as the arid zone genera The observed differences may indicate better thermoregulatory capacities in the arid zone species. These xerophilic species are exposed to a more variable thermal environment than the coastal forest species which experience thermal inertia. However, at high T8 (38 "C), P . tetradactylus regulated its T,, better than the arid zone species. This may be as a consequence of size, or only a short term effect. Although

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TRermaI biology of elephant shrews 65

Table 1. Thermal characteristics of elephant-shrews

PeImdmmUs Elephmmlm Elephmmh Elephantulus Elephanmlus Macmscelides Parameter t e t ~ ~ 1 u . s myurus edwonlii inhrfi btnchyhynetnu pmboscideur

Body m= (9) 206*5 65.2 f 1.2 49.8 46.5 f 2.6 45.3 f 1.7 38.8 Body t c n ~ p c r a t ~ ~ (“C) 33.1-37.5 37.2 37.6 33.5-37.7 34.2-37.7 34.9-37.8 Thlhcnnoncutrai m e (“C) 25-34 33-35 32.5-36.0 35 3s 37.5 Mean minimal VO, (ml 0, g1 h-I) 0.87 1.20 1.09 1.12 0.96 1.37 K expected VO, (K) 104 95.9 76.0 84.7 73 98

(HBL) 122 87.1 80.7 94 91 x intercept (T) 41.3 49.0 44.6 44.8 45.0 47.0 y intercept (%) 294 -400 -400 480 520 330 slope 0.049 0.089 0.097 0.120 0.1 13 0.079

-

Maxiium WEWL rh) 32.6 64.4 54.0 56.8 - 36.3

YD,, oxygen consumption; K. Kleibcr’s (1975) equation; H & L, Haysen & Lacy’s (1985) equation for eutherians; HEWL, maximum amount (%) of heat loss through evaporative cooling.

M. proboscideus is taxonomically distinct from the Elephantulus species, its Tb was comparable, which can be explained by adaptation to a similar thermal environment.

Thermal neutrality Temperatures defining the zone of thermal neutrality were highest in Macroscelides, generally intermediate in the Elephantulus species, and lowest in Petrodromus. The TNZ was higher in the more temperate Elephantulus species than in the tropical E. rufescens. Two of the most cold- adapted species, E. myurus and M. proboscideus, exhibited very narrow TNZs, whereas two tropical species, P. tetradaclyrus and E. rufiscens, showed broad TNZs. The temperate (higher latitude) species are exposed to much greater variation in both circadian and annual temperature variations. All species are exposed to high environmental temperatures during summer but only the temperate and arid zone species are exposed to subzero temperatures in winter, which also affects the location and range of the TNZ.

Oxygen consumption and metabolism All species showed the response characteristic of eutherian mammals, with VO, increasing significantly at Ta below the TNZ (Fig. 2). While YO, was stable above the TNZ in E. rufescens, it increased sIightly in P. tetraaktyius, and markedly in M. proboscideus and E. myurus. Again, this likely reflects differences due to size and latitude (between temperate and tropical species), rather than habitat (between mesic-and xeric-adapted species). The metabolic rates of all Elephantulus species were equivalent and only very marginally higher than that of Macroscelides. However, the specific rate of oxygen consumption was significantly lower in P. tetru&ctyIus than in any other species. M. proboscideus was the smallest species, and P. tetradactyius was the largest species studied. Because comparison of the predicted values should have accounted for mass specific differences (Kleiber, 1961; Hayssen & Lacy, 1985), the depressed metabolic rate of P. tetradactylus requires further explanation. It is associated with a continually warm to hot and very humid environment, reduced activity and resource abundance.

Respirometry and metabolic rates were mass specific, and predictable (usually f 10%) from allometric equations (Hayssen & Lacy, 1985) derived for eutherian mammals (Table 1). The VO, and BMRs of elephant-shrews are consistently higher than the mean values for insectivores, and slightly lower than the expected values for eutherians (Table 2). There was little variation in mean VO,consumption between all arid zone species of elephant-shrews over the range Ta = 5-35 O C .

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66 M.R Perrin

3

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32 !

Fig. 1. Mean body temperatures of (a) P. lebndacrylur (*), M. probarcidrw (+) and the Elephturlw species (m) over a range of ambient tcmpcraturrs. 0) Mean body temperature of E. rrrfescem (m), E. i n h j (+), E. bmchyrhynchus (*), E. edwlrvdii (0) and E myunu ( x ) .

With the exception ofP. tetra&ctylus, the predicted maximum Tb (intercepts with the abscissa) were higher than the recorded T,, particularly in E. mywus and M. proboscideus.' A high predicted Tb is indicative o f a species occupying a hot thermal environment. The depressed V0,s of E. brachyrhynchus and E intufi at Ta = 35 "C relative to the values for E. edwardi and E. myurn, are interpreted as an indicator of adaptation to a thermally stressed environment. Similarly, the relatively constant oxygen consumption of P. fetradactyltc, above the TNZ, particularly in E. rufescens, are indicative of adaptation to hot environments.

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Fig. 2. Mean rates of oxygen consumption of (a) P. tebodrcfylus (*), M. probarcideus (+) and the E ! e p h t u l u species (n) over a range of ambient tcmperaturcs. (b) Mean rates of oxygen consumption of (m), E. brcrchyrhynchus (+), E. mylvlu (*), E edwordii (0) and (E mfescens (x).

Thermal conductance Thermal conductance values were markedly dissimilar between Elephantulus species, thereby negating comparison with the other genera (Fig.3). The C, was extremely low in E. brachyrhynchus and E. intuf. In other elephant-shrews, C, increased slowly with T, until the TNZ was reached, whereupon rates of heat transfer accelerated rapidly. Responses were most marked in P. tetra&c@lus, E. myurus and E. ehuardii, while that of M. proboscideus was intermediate between those of the Elephantulus species, separating the western arid zone species pair,

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rn * 9 *

0

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Fig.3. Mean dry thermal conductance of (a) E. myunu (m), E. edwrdiii (f), f. tetr&c@lw (*), and M. probmcid=s (0) over a range of ambient temperatures. @) Mean dry thermal conductance of M. proboscideus (W), E. inafi (+) and E. bruc&/tyncchur ( x ) over a range of ambient temperatures.

Table 2. Percentage differences in the

elephant-shrews in relation to standard values for eutherians and insectivorans (Hayssen & Lacy, 1985)

Taxon Mocroscelides Elephantulus Petrodrows rates of thm

Eutherian Insectivoran 76

retr&c@lu proboscideus myrrnu

96 96 122 87 133

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Thermal biologv of elephant shrews 69

b 14

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Fig. 4. Mean evaporative water loss Of (a) p. tetrcrdcrcfylus (*), M. proboscideus (+) and the Elephuntulus species (H) over a range of ambient temperatures. (b) Mean evaporative water loss of E. mywur (8), E. bruchyrhynchus (+), E. intuft (*) and E. edwurdii (0) over a range of ambient temperatures.

E. brachyrhynchus and E. intufi, from the eastern mesic pair, E. myurus and E. edwardii. The high C, of E. myurus indicated considerable capacity to offload heat, and contrasts with the physiological characteristics of the arid zone species, E. brachyrhynchus and E. intufi. The general pattern of response, with increased conductance above the TNZ, and decreased conductance below the TNZ, was similar, and indicated effective vascular control of T, when EWL was low. This adaptive response was marked in P. tetradacvlus which, at Ta = 38 "C, maintained Tb below Ta.

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Minimal thermal conductance values for elephant-shrews approximate values predicted by allometric equations for other eutherians (Table 1).

Evaporative water loss With the exception of E. myurus, aspects of evaporative water loss were similar between species (Fig. 4). EWL was generally low and for most species approximated values characteristic of desert rodents. Most striking was the low EWL at high Ta in P. tetradactylus. This indicates that thespecies maintained a low Tb at high Ta, not through water loss, but through some other mecha- nism, probably peripheral vasodilation. Evaporative water loss is impossible in forest environments with high relative humidities and T.. However, EWL was also relatively low at high T. in species belonging to the other genera, as indicated by M. proboscideus and E. edwardii. The low rates of EWL are indicative of adaptations to avoid water loss in the Elephantulus species and M. proboscideus which inhabit arid zones or hot environments. The relatively high EWL of E. myurus at high T, indicates a propensity to offload heat in an environment where water is not scarce.

SPECIES ACCOUNTS Macroscelides proboscideus. Characterized by small size and a large surface to volume ratio, a BMR primarily determined by body mass, a high and narrow TNZ, a stable Tb, a moderate C, and a relatively low E WL (Roxburgh & Pemn, 1994; McNab, 1984).

Interpretation. The BMR is not reduced as in many arid zone andor insectivorous small mammals, but like desert gerbils and unlike other elephant-shrews, M. proboscideus is predominantly nocturnal and burrow-dwelling. These behavimrs enable avoidance of environmental extremes. The high level of Cmim is advantageous for a burrow dweller. It limits heat storage and prevents thermal death in a micro-environment characterised by high relative humidity (RH), but high RH prevents the efficient use of evaporative cooling. In dry surface air at high Ta EWL is moderate and contributes to offloading heat, however, it must be aided by conductance using peripheral vasodilation. Both physical and chemical means of temperature regulation are used. At low T, conductance is reduced which enhances insulation.

Water is conserved by low EWL, high urinz concentrating ability (UCA) (Downs & Pemn, 1995), hindgut resorption (Spinks & Pemn, 1995) and by behavioural responses to environmental changes.

Petrodrotnus tetradactylus. Large-bodied with a relatively small surface area; slightly elevated BMR, some lability in Tb; broad and low TNZ; extremely high conductance at high T, but very low EWL (McNab, 1984; Downs & Pemn, 1995).

Interpretation. The BMR characterizes a small mammal that is not resource limited. The position and width of the TNZ are not indicative of very high or very variable environmental temperatures, but are often associated with mesic habitats. Because the forest habitat is humid, cooling at high Ta is achieved by conductance, peripheral vasodilation and behaviour. Because evaporation is virtually impossible when ambient RH approaches saturation, alternatives to EWL are utilized. Exposure to only a narrow range of T. negates hyper- and hypothermia. The ecophysiology of P. terru&ctylus differs from that of most other elephant-shrews studied.

Elephantulus brachyrhynchus and E. intuf. (These species are treated together as they are physiologically inseparable.) Slightly labile Tb, characteristic (Macroscelid) TNZ, low BMR, steep VO, gradient, moderate to high EWL, very low dry thermal conductance (C.T. Downs & M.R. Perrin, unpublished data).

Interpretation. The slightly lowered BMR is interpreted as an adaptation to a dry, hot environ-

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Thermal biology of elephant shrews 7 I

ment where water and food resources are scarce. Body temperatures are precisely maintained at high T,. However, thmolability at lower T, may act as a buffer against widely fluctuating circadian Ta or indicate a propensity for torpidity. Insulation is extremely effective in conserving body heat at low T,; a necessity for a species exposed to low night temperatures in arid zone environments. The very low C, could lead to hyperthermia at high Ta, but evaporation in dry air is effective, and behaviour prevents exposure. Metabolic thermoregulation is more responsive to Ta than in any other elephant-shrew, but some water is required for EWL and cooling.

Unlike M. proboscideus which is a burrow dweller, and unlike E mpms and E. edwardii that use refugia in rocky outcrops, these species are exposed to low 7', in a their environment. While the habitat of E. in@ is more arid than that of E brachyrhynw, the latter species occurs at lower latitudes and might be exposed to an equivalent thermal environment.

Elephantulus myurus. Moderate size and predictable BMR, stable Tb in the laboratory, hypothermia occurs in the field; narrow TNZ; EWL and C, very high above the TNZ (Du Toit, Pemn & Fourie, in press).

Interpretation: Torpor has not been demonstrated in the laboratory but hypothermia occurs in the field. Further research is required on hypothermia and torpor in this species.

At low Ta, low C, is aided by shivering and non-shivering thermogenesis (NST) to effect insulation, whereas at high Ta Cd and EWL are greatly elevated to prevent hyperthermia. EWL is v e j effective in cooling the body at high Ta and accounts for 62% of metabolic heat production but can result in dehydration. The snout is licked to induce evaporation, is highly vascular, and contains tubular glands which are thought to offload heat (Kratzing & Woodall, 1985; Du Toit, 1993). Renal morphology and UCA indicate considerable capacity for water conservation (Downs & Perrin, 1995). These adaptations suggest a well-developed ability to physiologically regulate Tb at extreme Ta, and a capacity to survive in semi-arid environments.

Elephantulus edwardii. Low BMR, high Tb; broad and low TNZ; extremely high conductance at high Tas, but very low EWL (Leon, Shkolnik & Shkolnik, 1983).

Interpretation. Because the species is not deserticolous, it is speculated that the low BMR is correlated with herbivory and insectivory rather than aridity. At low Ta heat production is aug- mented by elevated Yo,, and peripheral heat loss is reduced by vasomotor control. Thermoregulation employs physical (heat transfer) and chemical (metabolic) processes. At high T, E m contributes significantly to heat loss although conductance is also markedly increased. Offloading heat includes panting, nose-licking, and vasodilation in the extremities. A low water turnover rate and high UCA (Downs & Pemn, 1995) conserves water and enables some cooling through EWL. A wide range of physiological and behavioural traits permit existence and survival in variable thermal conditions where water availability is seasonal, rather than scarce.

Elephantulus rozeti. Average size; low Tb below T. = 20 O C ; characteristic BMR; no data on C, or EWL (Seguignes, 1983).

Interpretation. E. rozeti is active throughout the year in rocky, arid areas ofNorth Africa Its Tb is labile, 32-37 "C in the field and 3 1-37 "C in the laboratory; it is dependent on T,, activity level and the availability of shade. Torpor shows a circadian pattern and occurs spontaneously. A critical Tb of 20 OC triggers arousal at a rate of 1 "C min-' between Ta of 20-34 "C. Torpor conserves energy efficiently and enables E rozeti to survive in a thermally extreme and fluctuating environment.

Elephantulus mJescenr. Average size; low Tb below T. = 20 "C; characteristic BMR; no data on C, or EWL (McNab, 1984).

Interpretation. Most thermolabile of the Elephantulus species; VO, and BMR as for other

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72 M.R. Perrin

Elephanrulus species; "NZ at T, = 35 O C ; VO, stable above the TNZ, but T, increases slightly. No data are available on C, or EWL.

CONCLUSION Elephant-shrews do not exhibit primitive characteristics in relation to their metabolism and thermal biology. Oxygen consumption is predictable from allometric equations for eutherians, and any depression in BMR is interpreted as an adaptive response to habitat variables, particularly aridity (availability of free water), relative humidity, and environmental temperature range. Stable T, are maintained over a wide range of environmental extremes and hyperthermia is contained even at high Ta. However, hypothermia is likely more common than is presently acknowledged owing to a lack of field data and focused laboratory research, the small size of elephant-shrews, their high metabolic rates, characteristic foraging behaviour (Lawes & Perrin, 1995) and exposure to low Ta diurnally and seasonally. Hypothermia has only been reported in E. myunrs (Du Toit ef al., 1995), while E. rozefi exhibits torpor (Seguignes, 1983).

Morphologically primitive mammals often have Tb that are more labile (Dawson, 1973) and/or lower than those of elephant-shrews. LOW or fluctuating T, are common amongst families of the Insectivora, including the Erinaceidae (T, = 34-35 OC; Shkolnik & Schmidt-Nielsen, 1976) and the Tenrecidae (Stephenson & Racey, 1993hb). The tupaiids, however, have low diurnal (35 "C) but high nocturnal (37 "C) T' (Bradley & Hudson, 1974; Whittow & Gould, 1976), while soricids have high Tb (Dawson, 1973). While the metabolic rates of macroscelids approximate those of tupaiids, they differ in maintaining stable high Tb at Ta below the TNZ, which is likely an adaptation to a colder natural thermal environment.

The relatively low BMRs of elephant-shrews can be explained by their preferred hot, dry habitats (McNab, 1979a). by their ant-eating habitats (McNab, 1984), or both. The metabolic and thermal characteristics of arid zone elephant-shrews parallel those of many desert rodents (McNab, 1979b; Downs & Perrin, 1990). Granivorous desert rodents including species ofthe Heteromyidae (McNab, 1979a; Hinds & MacMillen, 1985). Muridae (MacMillen, 1972; Shkolnik & Borut, 1969) and Cricetidae (Downs & Perrin, 1990) have lower than predicted BMRs. Energy needs and overheating are reduced, and consequently, water and energy are conserved (McNab, 1979b). Desert rodents and elephant-shrews that respond behaviourally to extreme climates, through the exploitation of mesic microenvironments and nocturnalism, uncouple thermoregulation from evaporative cooling (Bartholomew & Dawson, 1974). Water and energy budgets are balanced by reducing BMR or increasing UCA, or by a combination of both (McNab, 1979b).

The YO, values of arid zone elephant-shrews very closely approximate those recorded for the hairy-footed gerbils ofthe genus Gerbillurus which are arid zone small mammals endemic to southern Africa. In the five species of Elephanrirlus and the four species of GerbiIIurus studied (Downs & Pemn, 1990), VO, consumption approximates 3 ml 0, g'h- ' at T, = 10 "C and 1 ml0 , g'h-l at T, = 35 OC. Both taxa also exhibit similar patterns and levels of thermal conductance. In addition to occupying similar arid zone habitats, both species are predominantly insectivorous. However, elephant-shrews have approximately twice the average mass of Gerbillunrs species.

Although ant- and termite-eating mammals weighing more than 1 kg generally have low Tb and low BMRs, small insectivores possess relatively high metabolic rates (McNab, 1984). The relatively high basal rates in elephant-shrews ensure effective temperature regulation, but are partially offset by low food availability and a low energy density. In fact, 94% of the range in metabolic rate of ant-eating mammals is explained by the combination of body mass, food habits and the pres- encdabsence of burrowing (McNab, 1984). It is argued that ant-eating mammals, once evolved, are nearly impossible to displace ecologically, because much of ecological replacement is associated with high rates of reproduction, which are themselves correlated with high rates of metabo-

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lism in eutherians. Consequently, the ecological replacement of ant-eaters is inhibited because this food habit does not permit high rates of metabolism except at small mass. Elephant-shrews are small anteaters with high metabolic rates, but are extreme K-strategists, and energy commitments to reproduction are likely low, but sustained. They have persisted in the same niche over long periods of evolutionary time, which may be a consequence of myrmecophagy, their metabolic characteristics, and K-selection.

There is considerable scope for further research on many aspects of elephant-shrew ecophysiology, particularly on the Rhynchocyon species which remain unstudied. For Ekphuntufus species it is hypothesized that: the TNZ will increase positively with environmental Ta, and exhibit an inverse correlation with latitude (thermal stability of the environment); mean EWL will correlate positively with water availability (mean annual rainfall); and the incidence of lability in Tb will correlate positively with increased range in circadian and circannual environrnen- tal temperatures. Particularly fascinating will be energetic studies of the unique mode of locomo- tion of elephant-shrews, and much needs to be discovered about torpor, allantoin production, and the role of the tubular glands of the proboscis in peripheral vasodilation and heat exchange.

ACKNOWLEDGEMENTS I thank Colleen Downs-Wirminghaus for her helpful comments on the manuscript and Mrs Flockhart for typing it. The research was funded by the Foundation for Research Development and the University of Natal.

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APPENDIX 1

Metabolic rate and thermal biology In reviewing the thermal biology of elephant-shrews it is necessary to define some terms and con- cepts. Mammals require chemical energy to cany out various bodily functions which is referred to as energy metabolism. We estimate metabolic rate indirectly by determining oxygen consumption, because oxygen interacts in biochemical pathways with adenosine triphosphate (ATP) to liberate energy during cellular metabolism for the ongoing processes of living organisms. The determination of oxygen consumption (VO,) is a simple and practical measure of metabolic rate because the amount of heat produced for each unit litre of oxygen consumed approximates 4.8 kcal per litre 0, for most diets.

Because the rate of oxygen consumption varies with body size, we calculate the VO, per unit body mass, which is termed specific oxygen consumption. (Measurement is made on fasted and resting subjects to minimise variation in the metabolic rate.) In fact the rate of oxygen consumption per gram decreases consistently with increasing body mass (Schmidt-Nielsen, 1983) such that:

Specific oxygen consumption VO4 Mb = 0.676 x

where Mb = body mass in kg, and is expressed in litres 0, per kg body mass per hour (1 0, k g ' h-' equal to mi 0, g' h-I). This general equation is based on a wide variety of mammals ranging in mass fiom a fav grams to seved tonne. For example, a typical mammal of 1 kg body m a s can be expected to consume oxygen at about 0.7 I 0, per hour (Schmidt-Nielsen, 1983). However, metabolic rates, like other species traits, have evolved through natural selection in relation to environmental pressures, and can be higher or lower than the expected value for body mass. Data that relate VO, to body mass have been established for a variety of mammals, e.g. eutherians, marsupials, monotremes, ant-eating mammals, rodents etc. For example, marsupials generally have a body temperature (and mass specific metabolic rate) slightly lower than those of euthenans (by about 3 "C).

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76 M. R. Perrin

Although mammals are homeothermic and endothermic, species differ in the range of temperatures they can tolerate. Some have a very narrow, and others have a wide, tolerance range, which are correlated with habitat parameters, particularly the thermal environment.

Temperature accelerates many physiological processes, including metabolism and respiration. In general, a rise of 10 "C causes VO, to increase about two or threefold; the increase in rate is called the Q,, and is useful when comparing metabolic rates.

Heat balance For the body temperature (TJ of a mammal to remain constant, heat loss (Q) must equal heat gain (H). The amount of heat stored depends on the mean Tb, body mass, and the specific heat capacity of the tissues (Schmidt-Neilsen, 1983). Heat exchange, usually heat loss, between the body and environment takes place by conduction (including convection), radiation and evaporation, such that:

H, = f H, f Hr f He& H,

where, H, = metabolic heat production (always positive), H, = conductive and convective heat exchange (+ for net loss), H, = evaporative heat loss (+ for net loss), H, = evaporative heat loss (+ for net loss), H, = storage of heat in the body (+ for net heat gain by body). The three components of heat exchange depend on external factors, the most important ofwhich is temperature.

Temperature regulation in the cold Heat loss in the cold effectively takes place only through conduction (including convection) and radiation, because evaporation represents only a few per cent of total metabolic heat production, hence the equation is simplified:

H = C (Tb-Ta) (Schmidt-Neilsen, 1983)

where, C = thermal conductance, Tb = body temperature, Ta = ambient or environmental temperature. Therefore to maintain Tb constant at low T , adjustments have to be made to heat production (H) or conductance (C).

Heat production can be increased by muscular activity, shivering, and non-shivering thermogenesis. To clarify the role of heat production, consider the insulated body of a mammal with metabolic processes that generate heat, by burning oxygen, at the rate of H. Body temperature is therefore higher than the ambient temperature Ta. Ifthe environment becomes colder, Tb can only be maintained by increasing H proportionately to the difference between Ta and T,. The lower the T,. the greater the increase in metabolic rate, and oxygen consumption, to keep warm. Below a certain ambient temperature, called the lower critical temperature (TJ , the metabolic rate increases linearly with decreasing Ta (Fig. 1). Above the lower critical temperature, heat production, which cannot be reduced lower than the resting metabolic rate (RMR), remains constant as Ta increases until the upper critical temperature (Td is reached. This area between the Tk and T, defines the thermoneutral zone, where the metabolic rate is unaffected by changes in Ta. Its width is greater in temperate than in tropical mammals and the metabolic response to cold is more

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pronounced in temperate than in tropical mammals. When T, = T,, no heat is lost from the mammal, and no heat input is required to maintain T,; the

system is in equilibrium. The line (linear regression) that describes the heat production ofthe mammal relative to ambient temperature intersects with the abscissa when Tb = Ta (Schmidt-Neilsen, 1983). This intercept generates the expected maximum body temperature of the mammal.

Most tropical or hot-adapted mammals have TNZs between 20 and 30 "C (while those of temperate species are lower, and those of polar species are lower still), and the steepest regression lines. The slope of the line represents rhermul conducfunce (0. Generally tropical mammals have high conductances whereas temperate species have high insulation values. Consequently a tropical mammal, because of its high conductance (low insulation), must increase its metabolism significantly to maintain Tb for a relatively small drop in ambient temperature.

The location of the lower critical temperature, and the width of the thermoneutral zone, are not sufficient information about how well adapted a mammal is to its thermal environment. Informa- tion about the level of the resting metabolic rate, or better, the conductance values, is also necessary to evaluate the relationship between energy metabolism and heat regulation.

Torpor Maintaining Tb in the cold requires a severakfold increase in metabolic rate, which is expensive, so some small mammals allow their Tb to drop. This reduces the costs of homeothermy and econo- mises on the use of energy reserves. When T,, drops almost to T , the metabolic rate, heart rate, respiration rate and many other hnctions are greatly reduced, and the animal is said to be torpid. Daily periods of torpor are not uncommon in insect-eating small mammals, or those inhabiting montane or cold environments, even at relatively low latitudes.

Temperature regulation in the heat For T, to remain constant above the T, metabolic heat (BMR) must be lost at the same rate it is produced (Schmidt-Neilsen, 1983). From H = C (T,-TJ, we see that if H and Tb remain constant and T, changes, then the conductance term (C) must also change.

The conductance term refers to the total heat flow from the organism and can be increased in several ways. One way is by decreasing insulation to the skin (peripheral vasodilation) so that heat from the body's core is moved more rapidly to the surface; another is by exposing increased surface areas, especially naked or thinly firred areas, to a cool environment.

As Ta increases, the conditions for heat loss by conduction and convection (He) and radiation (HJ become increasingly unfavourable. Because metabolic heat production (H,) remains un- changed, the heat balance equation, H, = f H, f Hr f He f HI, must increasingly emphasize the evaporation (He) and storage (H,) terms (Schmidt-Neilsen, 1983). At high Ta evaporation is the key to heat balance, since if T, = Tb, there can be no loss of heat by conduction, and the net radiation flux approaches zero. To maintain constant T,, the entire metabolic heat production (H,) must be removed by evaporation.

The capacity for heat storage (HJ particularly in small mammals, is limited, and tolerance to increased Tb is finite. However, even a small increase in Tb can be important for a desert or semi- arid animal.

The total heat load, the sum of metabolic and environmental heat gain, is roughly proportional to the surface area of the body. This puts the small mammal, with its large relative surface area, in a far more favourable position with regard to heat load than a large mammal. Elephant-shrews with a body mass between 10 and 100 g have to evaporate water at a rate of 5-1 5% of their body mass per hour to maintain Tb. As a total water loss of between 10 and 20% is fatal for mammals (Schmidt-Neilsen, 1983), such rates of water loss can only be sustained for short periods. Most

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78 M. R. Perrin

desert small mammals evade the high temperatures behaviourally be retreating into burrows and or by being active at night.

Evaporative water loss (EWL), which is important for cooling, takes place from the upper res- piratory tract and from sweat glands on the skin surface. Elephant-shrews also spread saliva over their fur and lick their bodies to achieve additional cooling by evaporation.

Urine concentrating ability Although EWL is the major pathway for cooling small mammals at high TI, it is disadvantageous in that water is lost from the body. This could be critical, particularly in the tropics and deserts. However, many arid zone mammals conserve water by concentrating their urine, or by avoiding high TI behaviourally. Urine concentrating ability (UCA) and adaptation to high TI are often significantly and positively correlated with EWL.

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comparative aspects of the metabolism and thermal biology of elephant-shrews (macroscelidea)

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