Field Metabolic Rate in Two Species of Shrew-Tenrec, Microgale Dobsoni and M

Home , Microgale, Tenrec

Field metabolic rate in two species of shrew-tenrec, Microgale dobsoni and M. talazaci P. J. Stephenson, J. R. Speakman and P. A. Racey Department of Zoology, University of Aberdeen, Aberdeen, AB92TN, U.K.

Doubly labelled water (DLW) was used to determine field metabolic rate (FMR) in the shrew-tenrecs Microgale dobsoni and M. talazaci. Measures were obtained on six animals in their natural habitat and on five individuals in captivity. Mean FMR for nonreproducing M. dobsoni (mean body mass 42.6 ± 1.7 g) was 77.1 ±3.2 kJ/d (CV = 53.7%, N = 4), 3.8 times resting metabolic rate (RMR). Mean FMR for nonreproducing M. talazaci (mean body mass 42.8 ± 4.9 g) was 66.5 ± 14.1 kJ/d (CV = 51.9%, N = 6),3.2 times RMR. FMR within each species was not significantly correlated with body mass. This may in part reflect the large variation among individuals combined with the small sample size. FMR in shrew-tenrecs was within the range of FMR found in similar sized rodents, although variation was greater in the tenrecs. The high variability of FMR within the Tenrecidae may be a result of variations in body temperature. FMR/RMR ratios for both species fell within the range determined for other small mammals. The present study therefore offers further evidence to support a relationship between FMR and RMR.

Key words: Metabolic rate; Microgale dobsoni; M. talazaci; Doubly labelled water. Compo Biochem. Physiol. lO7A, 283-287, 1994.

Introduction The doubly labelled water (DLW) techni Many species within the Tenrecidae (Mam que (Lifson et al., 1949, 1955; Lifson and malia: Insectivora) do not maintain constant McClintock, 1966) enables an estimate of CO 2 homeothermy (Eisenberg and Gould, 1970; production, and hence daily energy expenditure, Nicoll and Thompson, 1987; Stephenson, 1991). in free-living organisms (for reviews see Nagy, .Therefore, metabolic rate measured under stan 1980; Speakman and Racey, 1988; Bryant, 1989; dard conditions for BMR is commonly referred Speakman, 1990). Energy expenditure measured to as resting metabolic rate or RMR (Nicoll in this way is commonly referred to as field and Thompson, 1987). RMR in many species metabolic rate (FMR). It has been suggested of tenrec fluctuates independently of body that total daily energy expenditure in mammals mass due primarily to fluctuations in body is proportional to basal metabolic rate (BMR) temperature (Tb ) (Stephenson and Racey, (McNab, 1980; Drent and Daan, 1980; Peterson 1993a,b). Daily and seasonal variation in et al., 1990; Koteja, 1991), with FMR being set RMR and T, also occurs (Stephenson, 1991; at a maximum of about four times BMR. This Stephenson and Racey, in press c) so FMR is supported by analysis of residuals from curves would be expected to fluctuate widely between of metabolic rate against body mass which show and within individuals. a strong correlation between relative BMR and We investigated FMR in two species of relative FMR (Daan et al., in press). shrew-tenrec, Microgale dobsoni and M. tala zaci. Both species have RMR lower than pre dicted from body mass (Stephenson and Racey, Correspondence to: Peter J. Stephenson, Department of Zoology, University of Aberdeen, Tillydrone Avenue, 1993b). The only previous study to apply Aberdeen AB92TN, U.K. Fax: 224 272396. the DLW technique on a tenrec investigated the Received 24 April 1993; accepted 28 May 1993 energetics of reproduction in captive pygmy

CPB(A) 107/2-8 283 284 P. J. Stephenson et at. hedgehog tenrecs, Echinops telfairi (Poppit, a variety of microhabitats such as herbaceous 1988). In the present study we aimed to study cover, tree roots and fallen logs. The plastic tenrecs in the wild in Madagascar. However, was pushed into the ground and tucked back the difficulties of retrapping study individuals below the leaf-litter root-mat layer to minimize meant most measures were taken on captive subterranean escape routes. The structure was animals or on semi-feral animals released into supported by trees and stakes of natural wood forest enclosures. We aimed to investigate the debris. Within the enclosures, tree trunks extent to which the field metabolic rates of and ground-lying branches were surrounded by M. dobsoni and M. talazaci are related to body plastic "collars" to block potential aerial run mass and RMR. ways. This was particularly important with M. talazaci which is semi-arboreal (Eisenberg Materials and Methods and Gould, 1970). Two nest boxes were placed in each enclosure. Tenrecs were introduced into M. dobsoni were captured from Reserve the enclosures via the nest boxes. Speciale (R.S.) Ambohitantely (l8°09'S, Animals were retrapped one or two nights 47°16'E) and M. talazaci were captured after initial injection. Lines of traps were laid from R.S. Analamazaotra (l8°28'S, 48°28'E) in the forest and up to 40 traps were placed in in Madagascar between January 1989 and each enclosure. The enclosure traps were February 1990. All tenrecs were trapped with checked every 2-3 hr during the night. Trap large Sherman mammal traps (H. B. Sherman lines outside the enclosures were checked each Traps Inc., Tallahasee, Florida, U.S.A.) baited morning at 0600-0800 hr. Recaptured animals with dried fish. The DLW technique was carried were reweighed and a second blood sample out on animals in their own habitat, although taken. All females used for DLW were taken measurements were also made on some individ back to Antananarivo and maintained in captiv uals held in captivity at the Pare Botanique et ity at Pare Tsimbazaza (see Stephenson and Zoologique de Tsimbazaza, Antananarivo. Racey, 1993b) to ascertain whether or not they Captured individuals were weighed, sexed had been pregnant during the study. and uniquely marked by ear-clipping. "Oxygen To measure background enrichment of in water (20.5 Atom Per cent Excess (APE), 180 and 2H, blood samples were taken from Yeda Research and Development Co. Ltd., individuals of the same sex, size and reproduc Rehovot, Israel) had previously been mixed tive condition as the study animals. Besides with deuterium (10 APE, Amersham Inter taking a blood sample from an animal before national, Little Chalfont, U.K.). The mass of injecting with DLW (which is impractical in DLW to be injected for each animal was esti small mammals), this is the most accurate way mated after Poppitt (1988) and was about 1% of of determining background isotope levels body mass. A 1ml syringe was filled with the (Speakman and Racey, 1987b). relevant volume of DLW (0.3-0.5 ml) and The 180 samples were prepared using the weighed to a precision of0.005 g using a White's guanidine technique (Speakman et al., 1990) torsion balance. The injection was administered and the 2H samples were prepared using intraperitoneally. uranium reduction (Wong and Klein, 1987). The syringe was reweighed immediately after Estimates of initial and final enrichments of 180 injection to determine mass of injectate. The and 2H were measured from duplicate samples study animal was then left undisturbed in a cloth using gas source stable isotope ratio mass spec bag for around 90 min to allow the isotopes to trometry (VG Isogas SIRA 9 and SIRA 10 mass reach equilibrium with body water (Speakman spectrometers). Estimates of CO2 production and Racey, 1987a). After this equilibrium period, were calculated using Equation 36 of Lifson an initial blood sample was taken from the tail and McClintock (1966) and converted to energy by removing the last 1-2 mm of skin with a sharp expenditure using the equation of Lusk (1976), scalpel. Blood was collected directly into 5 J..I.l assuming an RQ of 0.8. Mean values are pre capillary pipettes (Vitrex) which were sealed im sented in the text ± one standard error. mediately with a butane gas burner (Miniflam). The animal was then released. Results Since recapture rates for both species were low, enclosures were constructed at both study In the field, 13 individual M. dobsoni and 14 sites. These enclosures were barriers of trans individual M. talazaci were injected with DLW parent plastic sheet, 1-1.2 m high, erected and released. Of these, eight M. dobsoni (62%) around an area of forest (55 m2 at Ambohitan and four M. talazaci (29%) were recaught. tely and 20 m2 at Analamazaotra). Each enclo Of the 13 injected M. dobsoni released into sure was sited in the middle of known Microgale the enclosure at Ambohitantely, eight were habitat on relatively flat ground, incorporating recaught and of the five M. talazaci released Field metabolic rate in shrew-tenrecs 285 into the enclosure at Analamazaotra, two were to 20.1 kJjd. Therefore, mean FMR is 3.8 times recaught. Trap success was lower during the wet RMR. season (October-March) when animals were breeding and only two pregnant M. ta M. talazaci lazaci and one pregnant M. dobsoni were FMR in the field ranged from 32 to 80 kJjd trapped and injected with DLW. None of these (N = 3) compared with 40-124 kJjd (N = 3) in was recaptured. Sample loss during gas analyses captivity, but there was no significant difference meant that FMR was determined under natural in mean FMR (W = 9.0, P > 0.05). Captive conditions for only three M. dobsoni and three animals were not significantly heavier than M. talazaci. wild animals (W = 6.0, P > 0.05). Mean FMR In addition to field studies, six M. talazaci pooled across all non-reproducing adults (mean and six M. dobsoni were injected with DLW in body mass 42.8 ±4.9 g) was 66.5 ± 14.1 kJjd captivity at Pare Tsimbazaza, Antananarivo. (CV = 51.9%, N = 6). This represents 3.2 times These included a single pregnant female and a RMR, which is 21.0 kJjd (Stephenson and single lactating female of each species. However, Racey, 1993b). FMR was not related to body sample loss during gas analyses resulted in only mass (P > 0.8, r 2 = 0.02). five measures being obtained from these captive tenrecs: two for M. dobsoni and three for Discussion M. talazaci. The only previous study to use the DLW M. dobsoni technique on tenrecs was Poppitt (1988) who At Ambohitantely, energy expenditure in non studied E. telfairi during reproduction. FMR reproducing M. dobsoni varied between 21 and ranged from 35 kJjd to 110kJjd (mean 65 kJjd, 106kJjd (N = 3). In captivity in Antananarivo, a N = 6) in pregnancy and from 24 to 65 kJjd nonreproducing female had FMR of 110kJjd, (mean 48 kJjd, N = 9) in lactation. The lowest whereas a lactating individual had FMR of mean level of FMR was 37 kJjd in late lactation 239 kJjd (Fig. I). FMR was not significantly (Poppitt, 1988). different between animals measured in the field Poppitt (1988) provides no measure of FMR and animals measured in captivity (Mann-Whit in nonreproducing E. telfairi but the mean ney U'-Test: W = 6.0, P > 0.05). Although cap values in reproduction are lower than values tive animals were generally heavier, their body determined here for nonreproducing individuals mass was not significantly different (W = 6.0, of both species of Microgale. This is surprising P > 0.05). The mean energy expenditure pooled since the mean mass of E. telfairi is much across all the nonreproducing animals (mean greater (e.g. 262.8 g in lactation) (Poppitt, body mass 42.6 ± 12.1 g) was 77.1 ±41.4 kJjd 1988). The low level of FMR in E. telfairi (CV = 53.7%, N = 4). FMR was not related to may reflect the captive conditions in which body mass (P > 0.5, r 2 = 0.10). Mean RMR for the animals were kept. Housed in cages and

M. dobsoni is 41.7 ml02jhr (Stephenson and maintained at a constant ambient temperature, Racey, 1993b). Converting oxygen consumption costs of thermoregulation and activity would to kJjd, assuming an RQ of 0.8 and hence be reduced. However, compared with other 20.097Jjml02 (Lusk, 1976), RMR is equivalent eutherians, FMR in desert-dwelling mammals is reduced by around 30% (Degen et al., 1986; Nagy, 1987). Since E. telfairi originates from the 300 arid south-west of Madagascar, its relatively lactating female low FMR may reflect an adaptation to this • environment. In contrast, the two species of 200 Microgale in the present study are eastern and central forest-dwelling tenrecs. ~ In E. telfairi, Poppitt (1988) found large ~ • variation in FMR within and between individ 100 c • 0 uals and coefficients of variation at different I:l • stages of reproduction ranged from 47.1% to 0 0 c • 59.5%. In other small mammals measured 0'------1.----'----'---"-----' using DLW, CV has been less, e.g, 24.5% in 20 30 40 50 60 70 the pouched mouse, Saccostomus campestris Body mass(g) (Speakman et al., 1992), 12.2% in pregnant little brown bats, Myotis lucifugus (Kurta Fig. I. Field metabolic rate (FMR) in M. dobsoni (square symbols) and M. talazaci (circles). Individuals measured in et al., 1989), 7.6%-18.5% in the common the field or semi-feral conditions represented by open sym shrew, Sorex araneus (Poppitt, 1988) and bols. Captive individuals represented by closed symbols. 15.9%-30.1 % in the white-footed mouse, 286 P. J. Stephenson et al.

Table I. Mean FMR of Microgale dobsoni and M. talazaci compared with some other small mammals Body mass FMR Species (g) (k.l/d) FMR/RMR Source Insectivora Microgale dobsoni 42.6 77.1 3.8 This study Microgale talazaci 42.8 66.5 3.2 This study Echinops telfairi 262.6· 37.0· 1.3 Poppitt 1988 Sorex araneus 11.1 70.1t 2.6 Poppitt 1988; Gebczynski 1965 Rodentia Dipodomys merriami 35.9 61.8 3.1 Yousef et al. 1974; Mullen 1971a Dipodomys microps 58.6 117.4 3.8 Yousef et al. 1974; Mullen 1971a Acomys cahirinus 38.3 51.8 2.5 Hayssen and Lacy 1985; Degen et al. 1986 Acomys russatus 45.0 47.6 2.7 Hayssen and Lacy 1985; Degen et al. 1986 Peromyscus crinitus 13.4 40.1 4.0 Hayssen and Lacy 1985; Mullen 1971b Chiroptera Macrotus californicus 13.0 22.8 3.1 Bell et al. 1986 Plecotus auritus 7.5t 19-25· 3.2 Speakman and Racey 1987a ·Late lactation. tEarly pregnancy.

Peromyscus leucopus (Randolph, 1980). There Considering rodents of similar size to the two fore, although there is generally large variation Microgale species (Table 1), there is great vari in measures of FMR, in the Tenrecidae this ation among species but mean FMR in tenrecs variation appears to be greater than for other is within the range determined for rodents. mall mammals. Across all small mammals studied (Table 1; Poppitt (1988) suggested that the variation in Koteja, 1991), the ratio of FMR to RMR is not FMR in E. telfairi "may be due to variation related to body mass. This suggests that both in maternal body temperature", with animals values scale to a similar exponent and give a maintaining homeothermy having higher energy constant usually between three and four. expenditure. A similar phenomenon has been lt has been suggested that daily energy expen noted in the study of FMR in bats (Speakman diture is directly related to RMR (e.g. McNab, and Racey, 1987a). In the present study, vari 1980; Drent and Daan, 1980). There is evidence ation in FMR may also be a result of variations that the maximum ceiling of sustained energy in body temperature since T b in both species is expenditure, and therefore the limit to daily influenced by T, (Stephenson and Racey, 1993b). energy expenditure, is limited to within six times Further work is required to ascertain the re RMR in mammals (Peterson et al., 1990) and lationship between Ta , T, and FMR in tenrecs. seven times RMR in birds (Bryant and Tatner, Nagy (1987) and Koteja (1991) have reviewed 1991). Recent evidence suggests that the mor data available on FMR in eutherians and phological apparatus required to sustain daily marsupials, as well as in birds. They found energy expenditure will be maintained by resting that FMR is strongly correlated with body mass metabolism so that FMR and RMR will be at an interspecific level in all study groups. inherently linked (Daan et al., in press). This is The lack of relationship between FMR and supported by analysis of residual values from body mass in the present study may be a metabolic rate-mass curves which show a strong factor of small sample size or it may reflect correlation between relative RMR and relative differences in interspecific and intraspecific FMR (Daan et al., in press). The present study scaling patterns. However, the lack of relation offers further evidence to support the relation ship may also be due to the inherent variability ship between FMR and RMR. in FMR and the fact that the larger individuals were captive, and therefore, restricted in their Acknowledgements-We would like to thank the govern ment of Madagascar for permission to conduct this study. locomotor activity. We are especially grateful for the help and collaboration Most studies of eutherian FMR have concen of the Departement des Eaux et Forets, Mme. B. Rakoto trated on rodents and there has been only one saminanana, the Ministere de l'Enseignement Superieur, measure of FMR in an insectivore outside the and Dr V. Randrianasolo and staff at Pare Tsimbazaza. Tenrecidae. Poppitt (1988) measured FMR in Support from the WWF-Aires Protegees team was invalu able, and we are especially grateful for the help and advice the shrew Sorex araneus during reproduction. of Dr M. E. Nicoll. Field and laboratory assistance FMR in early pregnancy was 70.1 kJ/d (Poppitt, came from F. Rakotondraparany, N. Rakotoarison, 1988). This is higher than the mean FMR H. Randriamahazo and E. Rasoarimalala, In the U.K. we in many other small mammals, even those of thank Dr A. Fallick and staff at the Scottish Universities Research and Reactor Centre, East Kilbride, for their greater body mass (Table I). This coincides with assistance during isotope analyses. The work was funded by the especially high RMR found in the Soricidae a Natural Environment Research Council studentship to (Vogel, 1980). PJ.S. Field metabolic rate in shrew-tenrecs 287

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