J . Zool., Lond. ( 1993) 231, 179- I86

Poikilotherinic traits and thermoregulation in the Afrotropical social subterranean Mashona mole-rat (Crjytoniys hottentotus d a r h g i )

(Rodentia: Bathyergidae)

(With 2 figures in the text)

('ontents

I'agc 1 nt rod tict ion . . . . 179 Materials and iiicthods . . . . . . . . . . . . . . . . . . . . . . . . . . I XO

Exprlriniciitalpi-ocejurc . . . . . . . . . . . . . . . . . . . . . . 180 Resulls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I X I Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I82 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I 8 5

. . . . . . . . . . . . . . . . . . . . . .

Expcrimen t B I a iii mals . . . . . . . . . . . . . . . . . . . . . . . . . . 1x0

I iitroductioii

The Mashona mole-rat ( C r ~ ~ ~ p ~ o i n ~ ~ s h l ~ f t C i ? / O f L L S titi/.lingi) is 21 social subterranean rodent showing a reproductive divisioii o f labour similar 10 other spccica and stibspecieh ol'the genus (Bennett. 1988. 1989, 1990; Hcnnctt & Jarbis, 10x8). In each colony o n l y one female will reproduce.

The burrows o f C ' . 11. t l r i i . / i r y i tend t o be constructcd i n compact sandy clay soils. The burrow systems are sealed from the suiface and consist of tiuiiici~otts long subsurface I'oraging tunnels & 25 cni deep and a deeper ( +30 c m ) cciitral area more pi-otcctcd from predators and temperature extremes (Bcnnett, Jarvis & Davies, 1988). The Maahona inole-rat rarely vcntures above ground and thcrefore lives in a buffered thermal environment.

I79

< ' 1993 The Loological Society o f London

180 N. C. BENNETT, J . U. M . JARVIS A N D F. P. D . COTTERILL

The available literature on metabolism in subterranean rodents has shown that they characteristically exhibit lower resting and basal metabolic rates than above-ground rodents of comparable size (McNab, 1979; Lovegrove, 1986a, 6). These low RMRs may be an adaptation to hypoxia and hypercapnia (Arieli, 1977; Arieli et al., 1984) and may also be energy-saving adaptations to offset the great energetic cost of burrowing (Jarvis, 1978; Vleck, 1979, 1981; Lovegrove, 1987).

Recent evidence has shown that some social subterranean bathyergids display RMRs higher than those of solitary bathyergids or solitary subterranean rodents but, nevertheless, still lower than most above-ground rodents (Buffenstein & Yahav, 1991; Bennett, Clarke & Jarvis, 1993). This paper reports poikilothermic traits between the relationship of Tb against Ta. The RMR, thermal neutral zone and thermal conductance of the Afrotropical Mashona mole-rat of Zimbabwe are presented. In addition, further evidence is provided to show that most social subterranean bathyergids indeed possess higher RMRs than solitary species.

Materials and methods

Experimental animals

Seven Cryptomys h. darlingi (2 females and 5 males) from a single colony were collected at Goromonzi (17" S, 3 1'' E) in Zimbabwe. Body mass (M) of the individuals ranged between 39 and 93 g (60 f 16.4 g). The mole-rats were housed together in a single glass terrarium in a constant temperature room at 26°C. Wood shavings and paper towelling were provided as nesting material. The mole-rats were fed on a variety of vegetables, supplemented weekly with a high protein PronutroR cereal.

Experimental procedure

Air flow rate (cm3/min) to the respirometer was determined using a bubble flowmeter constructed of a modified burette containing soap water. The respirometer (in which the animal was housed) consisted of a cylindrical transparent Perspex chamber (800 cm') fitted with 6-mm diameter inlet and outlet ports. Temperatures were kept constant within the respirometer by placing it inside a small (0.11 m') temperature- controlled cabinet. A negative pressure flow-through system was used. Outside air was pulled through the respirometer, scrubbers (COz trap of soda lime and water trap (of colour-indicator silica gel)) and oxygen analyser at a flow rate of 370-378 cm' min-I.

The techniques of Bartholomew, Lighton & Louw (1 985) and Lighton (1985) were used to measure the rate of oxygen consumption (VO,) with an Applied Electrochemistry S-3A 2-channel oxygen analyser connected to a British Broadcasting Corporation microcomputer. This procedure records the voltage between the fractional concentrations of oxygen in the respiratory and calibration streams (Lovegrove, 1987). VOz expressed as a mass-specific rate was calculated according to Depocas & Hart (1957) as:

where F102 is the 0 2 fraction of the inlet air and F20, the fraction of the outlet air, before and after the chamber was connected to the measuring circuit. 002 is expressed as cm3 0, g-' h- ' and V2 is volume in cm3 air h-' . Values were corrected to S.T.P. conditions.

The progress of each run (an experiment lasting up to 3 h) was visually monitored on a Visual Display Unit, and markers were placed on the trace to correspond with behavioural observations made during the run. Each run lasted 180 min, with data points collected every 17 sec. The initial 30 min of the run were used to allow the animal to settle, and consequently this section of the trace was not analysed.

POIKILOTHERMY A N D THERMOREGULATION I N T H E MASHONA MOLE RAT 181

A portion of the trace of approximately 20 min in length, corresponding to the lowest stable oxygen consumption when the mole-rat was calm and completely at rest, was integrated, averaged and calculated in cm' O2 g-I h-I (S.T.P.), and presented as the mean kS.D. for each respective Ta. However, at lower temperatures (1 8 and 21 'T) portions of the trace of approximately 5-1 0 min in length were used because the mole-rats were reluctant to rest for longer periods of time.

The relationship ofVOz and Ta, when Ta was below the lower limit of thermoneutrality (TI) was analysed using the method of least squares (Zar, 1984). Conductance (Cm) below TI was calculated from individual measurements of VO, using the formula Cm=VO>/(Tb-Ta) (McNab, 1980) and presented as the mean +. S.D. in cm' O2 g h ~ ' 'C- ' . The points were further converted to the thermal units of conductance mW/'C. The thermal conductance allows a measurement of the heat which is exchanged between the body and the environment.

The experiments were run 08:OO h to 18:OO h to lessen the elTects of any potential endogenous rhythms of metabolism.

The animals were deprived of food for 3 h prior to measurement of metabolic rate in order to achieve a post-absorptive state and reduce the influence of specific dynamic action. Body (rectal) temperature (Tb) and ambient temperatures (Ta) were measured using copper-constantan thermocouples (2 mm diameter). For the rectal temperature measurements, the copper-constantan thermocouple was inserted 1.2 cm into the animal's rectum after the mole-rat had been left for 2 h at the required Ta in the temperature-controlled cabinet. To avoid undue stress a t the upper and lower extremes of temperature, the mole-rats were only left in the cabinet for 1 h.

Oxygen consumption was not measured below 18 ;C, because the molc-rats invariably rested for too short a time period to get a meaningful VO2.

Results

The body temperature of C. h. durlingi remained stable at Tas from 25-31.5 'C with a mean value of 33.3 k 0.5 "C (n = 28). Above 33 'C, T b increased to a mean of 34-7 0.77 "C (n = 28) (Ta range 33-39 "C). Below 25 "C the relationship between Tb and Ta shows a poikilothermic trait, with body temperatures dropping 21 ' X I of the value expected for normal homeo-thermoregulation (Fig. 1). The drop in Tb with decreasing Ta is given by the equation Tb = 24.12+0.366 Ta (n =42, r2=0.82, P<O.OOI) .

The mean RMR of acclimated C. h. d d i n g i was 0.98f.0.14 cm' 0 1 g- ' h- ' (n=21) within a thermoneutral zone of 28G31.5 "C (Fig. 2). Below the lower limit of thermoneutrality, the increase in metabolic rate is given by the equation V 0 2 = 5.6003-0.1652 Ta (n = 28, r2 = 0.77, P < 0.00 I ) . The conductance was high 0.19+0.03 cm' 0 2 g- ' h - I 'Y- ' (n=28) at the lower limit of thermoneutrality when compared to other bathyergid mole-rats. The conductance of a Mashona mole-rat of mean body mass 60 g and assuming a RQ of 0.8 was 63.4 mW.

The mean metabolic rate at I8 "C, the lowest Ta used to obtain an oxygen consumption, was 2.63 f0.55 cm3 0 2 g-l h-' which is 2.6 times that of the RMR in the TNZ.

The Mashona mole-rat was unable to maintain a stable Tb below thermoneutrality. Heat production (HP) increased over the ambient temperature range 25-1 8 "C below T1. The increase in heat production, however, was not sufficient to offset the greater heat loss induced by the lower ambient temperature; hence Tb fell.

The oxygen consumption of the reproductive female was generally much lower than that of the other colony members, especially below TNZ (Fig. 2).

182

38 -

36 -

34 -

N . C. B E N N E T T , J . U . M . JARVIS A N D F. P. D. COTTERILL

s - 32-

?!

2 3 I

30-

c E - 3 28- 0

~ m

. I : t ..

24 -

261 ' !

!

* i

! - .

FIG. 1. Body temperature (rectal) of seveii Mashoiia mole-rats, CrjyfomFs h. d d i n g i , as a function of ambient temperature. Each solid dot (0 ) represents a rectal temperature at the prescribed arnhient temperature. The solid line (m-w) of Ta vs. Tb represents a true poikilothermic relationship.

Discussion

Subterranean rodents spend their lives underground in sealed burrows and rarely come to the surface (Nevo, 1979). These animals show considerable specialization. Morphological, anatomi- cal and physiological adaptations in mole-rats permit efficient burrow excavation, foraging and soil movement in their underground ecotope (Eloff, 1958; Lovegrove, 1987; Jarvis & Bennett, 1990, 1991).

Foraging burrows are shallow (c. 25 cm depth), and the temperatures experienced in these burrows represent the extremes to which the mole-rats are exposed in the field. The daily and annual amplitude in temperature fluctuation is greatest at the soil surface, diminishing with increasing depth. Mean annual soil temperatures in the burrows of rodent moles vary minimally at depths exceeding 0.6 m (Bennett, Jarvis & Davies, 1988).

McNab ( 1 979) and Lovegrove ( 1 9860) have shown that subterranean rodents display distinct physiological traits such as low body temperatures, low RMRs and high conductances. The Mashona mole-rat exhibits two of these three metabolic adaptations but, in common with some of the other social bathyergids, has a high RMR (Buffenstein & Yahav, 1991; Bennett, Clarke & Jarvis, 1993).

In contrast to previous reports on RMRs of bathyergids (Lovegrove, 1986u,h, 1987), C. h. durlingi (this study) and C. h. hottentotus (Bennett, Clarke & Jarvis. 1993) have markedly higher RMRs more reminiscent of some RMRs recorded for geomyids, spalacids and the solitary

P O I K I L O T H E R M Y A N D T H E R M O R E G U L A T I O N I N THE M A S H O N A M O L E R A T 183

\

0 / . . . . . .

20 22 24 26 28 30 32 34 36 38 Ambient temperature ("C)

F I G . 2. Oxygen consumption (V02) of seven Crq~on7,1:~/1. drrrling, as a function of ambient temperature. Each solid dot ( 0 ) represents a single oxygen measurement on a mole-ral. The open dot (0) represents VOz for the reproductive female. The solid squares (H-H) represent the mean oxygcn consumption at the prescribed ambient temperature.

occurring bathyergid Heliophohius urgmrcocinereus (Table 1) (Pearson, 1947; Bradley, Millar & Yousef, 1974; Nevo & Shkolnik, 1974; Bradley & Yousef, 1975; McNab, 1979). The social bathyergid C. dumurensis, a markedly larger animal than the other members of the genus Crjytomj.s, does not fit this pattern, hence the RMRs in the two subspecies of Cryptomys hottentorus may be an allometric consequence of the body size of these small animals (Bennett, 1989; Bennett, Clarke & Jarvis, 1993). I t is of interest that the oxygen consumption by the reproductive female in the colony was generally much lower than the other colony members, especially below TNZ. This is of significance because she was an average-sized animal (58 g). It is possible that this is a physiological adaptation for the energetically costly process of producing the young.

The Mashona mole-rat has the lowest body temperature of all the haired bathyergids recorded to date, but is higher than the naked mole-rat which exhibits true poikilothermic traits (Table I). It

TA

BL

E I

Mea

n bo

dy m

ass,

rest

ing

met

abol

ic r

ate,

bod

y te

mpe

ratu

re a

nd s

ocia

l st

atus

of s

elec

ted

subt

erra

nean

rod

ents

Spec

ies

Fam

ily

Het

eroc

epha

lus

glab

er

Cry

ptom

ys h

. dar

lingi

C

rypt

omys

h. h

otte

ntot

us (

N. C

ape)

H

elio

phob

ius

arge

nteo

cine

reus

C

rypt

omys

h. h

otte

ntot

us (

Tra

nsva

al)

Cry

ptom

ys d

amar

ensi

s G

eory

chus

cup

ensi

s B

athy

ergu

s jar

ietta

B

arhy

ergu

s su

illus

Sp

alax

ehr

enbe

rgi 2

1152

-60

Spa

lax

leuc

odon

Th

omom

ys ta

lpoi

des

Geo

mys

bur

sari

us

Bat

hyer

gida

e B

athy

ergi

dae

Bat

hyer

gida

e B

ath y

ergi

dae

Bat

hyer

gida

e B

athy

ergi

dae

Ba th

yerg

idae

B

athy

ergi

dae

Bat

hyer

gida

e Sp

akdc

idae

Sp

alac

idae

G

eom

yida

e G

eom

yida

e

39.5

60

75

88

95

I2

5 18

1 40

6 62

0 11

6-12

1 15

1 10

5 19

7

RM

R

cm'

g-'

h-'

0.64

-1.0

0 0-

98

0.9-

1.3

0.85

0.

68

0.57

-0.6

6 0.

59

0.53

0.

49

0.62

-0.9

5 0.

84

1.22

0.

70

Bod

y te

mpe

ratu

re

in T

NZ

("C

)

32

33

34

35

35.8

35

36

.4

34.8

35

35

-36

37

35.5

36

Soci

al

stat

us

soci

al

soci

al

soci

al

solit

ary

soci

al

soci

al

solit

ary

solit

ary

solit

ary

solit

ary

solit

ary

solit

ary

solit

ary

Hab

itat

(d

egre

e of

ra

infa

ll)

sem

i-ar

id/a

rid

sem

i-ar

id

sem

i-ar

id

mes

ic

mes

ic

sem

i-ar

id/a

rid

mes

ic

sem

i-ar

id/a

rid

mes

ic

mes

ic/s

emi a

rid

mes

ic

mes

ic

mes

ic

Ref

eren

ces

McN

ab,

1979

, Buf

fens

tein

& Y

ahav

, 19

91

Ben

nett,

Jar

vis

& C

otte

rill,

thi

s st

udy

Ben

nett,

Cla

rke

& J

arvi

s, 1

993

McN

ab,

1979

H

aim

& F

aira

ll, 1

986

Lov

egro

ve, 1

986~

; Ben

nett,

Cla

rke

& Ja

rvis

, 199

3 L

oveg

rove

, 198

7 L

oveg

rove

, 198

66

Lov

egro

ve, 1

9866

N

evo

& S

hkol

nik,

197

4 M

cNab

, 19

73; B

radl

ey e

t ul.

1974

B

radl

ey e

t al

., 19

74

Bra

dley

& Y

ouse

f, 19

75

POIKILOTHERMY A N D THERMOREGULATION IN THE MASHONA MOLE RAT 185

is of extreme interest that below 25 "C C. h. darlingi experiences problems in maintaining a stable core body temperature. This may be due to the small body mass c. < 60 g of these mole-rats (thus increasing the surface/volume ratio) coupled with a high conductance. When in thermal equilibrium, Ta and Tb can be regulated by balancing heat loss (HL) with heat production (HP). Below 25 C, despite a marked increase in oxygen consumption below thermoneutrality (up to 260'!h at 18 C), the increase in HP of C . h. darlingi is sufficient to maintain a constant Tb over the range 25-1 8 "C. The high conductivity in the Mashona mole-rat may also account for the high heat tolerance (c. 39°C) exhibited by this animal, which would otherwise kill the Damaraland mole-rat, C. dumarensis (N. C. Bennett, unpubl.). The high conductance exhibited by this animal may be an adaptation for facilitating heat loss in the humid burrow systems.

Bennett, Clarke & Jarvis (1993) have shown that C. h. hottentotus experiences a homeothermic relationship of Tb with Ta; this suggests that the increased conductance in C. h. darlingi is responsible for the poikilothermic enigma. But how does this arise? The Mashona mole-rat, like the naked mole-rat, occurs in the tropics of Africa, where seasonal changes in climatic conditions are muted in comparison to those experienced in the temperate and subtropical arid zones inhabited by C. h. hottentotus and C. damarensis, respectively. It is of interest that both species exhibiting poikilothermic traits are small-sized animals from the tropics. In the burrow system of the naked mole-rat, conditions are relatively stable throughout the year with a die1 temperature range of less than 2 "C (Bennett, Jarvis & Davies, 1988) and similar seasonal constancy (Gorou, 1970). We would speculate that the burrow system of C. h. darlingi would experience a similar temperature range. The constancy of the burrow thermal regime and the selection for this ecotope may explain why, below the lower critical limit of thermoneutrality, the Mashona mole-rat shows an inability to thermoregulate like a true homeotherm.

Within the social Bathyergidae are found homeothermic species Cryptomys hottentotus hottentorus and Cryptomys damarensis (Lovegrove, 1986a; Bennett, Clarke & Jarvis, 1993) and the poikilothermic naked mole-rat, Heterocephalus glaber (McNab, 1980; Buffenstein & Yahav, 1991). The Mashona mole-rat appears to bridge the gap between these two extremes by being a poorly thermoregulating endothermic animal.

We thank Pierre Janssens and Gonzalo Aguilar for assistance with the taking of rectal temperatures. Dr Rochelle Buffenstein, Miss Caroline Rosenthal and two anonymous reviewers are thanked for critically reviewing the manuscript. We are grateful to the Department of National Parks and Wildlife Services, Harare, Zimbabwe for permits to trap and export the mole-rats from the Republic of Zimbabwe. The study was financed by research grants from the University of Cape Town and the Foundation for Research and Development to JUMJ and NCB.

REFERENCES

Arieli, R. (1977). The atmospheric environment of the fossorial molerat spa la.^ ehrenberzi): effects of season, soil texture, rain. temperature and activity. Comp. Biochem. Physiol. (A) 63: 569-575.

Arieli, R., Arieli, M., Heth, G. & Nevo, E. (1984). Adaptive respiratory variation in 4 chromosomal species of mole-rats. Experientia 40: 512-514.

Bartholomew, G. A,, Lighton, J. R. B. & Louw, G . N. (1985). Energetics of locomotion and patterns of respiration in tenebrionid beetles from the Namib desert. J . comp. Physiol. 155 155-162.

Bennett, N. C. (1988). The trend towards sociality in three species of southern African mole-rats (Bathyergidae): causes and consequences. PhD thesis, University of Cape Town, RSA.

Bennett, N. C. (1989). The social structure and reproductive biology of thecommon mole-rat, Cryptomys h. hottentotusand remarks on the trends in reproduction and sociality in the family Bathyergidae. J. Zool., Lond. 219: 45-59.

I86 N . C. BENNETT. J . U. M . J A R V I S A N D F. P. D . C O T T E R I L L

Bennett, N. C. (1990). Behaviour and social organization in a colony of the Damaraland mole-rat Crypfoi?iy.v damarmvi.s.

Bennett, N. C. & Jarvis, J . U. M. (1988). The social structure and reproductive biology ol‘ colonies of the mole-rat

Bennett, N. C . , Jarvis, J. U . M. & Davies, K . C. (1988). Daily and seasonal temperatures in the burrows of African rodent

Bennett, N. C., Clarke, B. C. & Jarvis, J. U. M. (1993). A comparison of metabolic acclimation in two species of social

Bradley, W. G., Miller, J. S. & Yousef, M. K. (1974). Thermoregulatory patterns in pocket gophers, Geom.v.s hursariu.,:

Bradley, W. G. & Yousef, M. K . (1975). Thermoregulatory responses in the plains pocket gopher, Gromys hursurius. Comp.

Buffenstein, R. & Yahav. S. ( 1991). Is the nakcd mole-rat. Hetc~roc~c~plzulu.s gluhcv an endothermic yet poikilothermic

Depocas, F. & Hart, J. S. (1957). Usc of the Pauling oxygen analyser for measurement of oxygen consumption of animals in

Eloff. G. (1958). The functional and structural degeneration or the eye of the South African rodent moles. Cryptowiys

Gorou. P. (1970). L’Afrirpr,. Paris: Hatchett. Ifaim. A. & Fairall. N . ( 1 986). Physiological adaptations to the subterranean environment by the mole-rat Crypfc’n!),.s

h 0 / /m lo I us. (‘ir?7hcht/.Sif/ 8 49 5 3 Jarvis, J. U. M. (1978). Energetics of survival in Heterocephalus gluher (Ruppell), the naked mole-rat (Rodentia:

Bathyergidae). BUN. Curn. Mus. Nut. Hist. 6 81-87. Jarvis, J. U. M. & Bennett. N. C . (1990). Theevolutionary history, population biology and social structure of African mole-

rats: Family Bathyergidae. f r o g . Clin. B id . Rex 335: 97--128. Jarvis, J . U. M. & Bennett, N. C . (1991). Ecology and behavior of the Family Bathyergidae. In The hio1og.v of the nukrd

mole-rat: 66-97. Sherman, P. W., Jarvis, J. U. M. &Alexander, R. D. (Eds). Princeton, USA: Princeton University Press.

Lighton, J. R. B. (1985). Minimum cost of transport and ventilatory patterns in three African beetles. Phj’siol. Zool. 58: 390-399.

Lovegrove, B. G . (1986~). The metabolism of social subterranean rodents: adaptation to aridity. Oecolugiu 6 9 551 -555. Lovegrove, B. G. ( 1 986h). Thermoregulation of the subterranean rodent genus Bath-yergus (Bathyergidae). S. Afr. J . Zoo/.

Lovegrove. B. G. (1987). Thermoregulation in the SUbterrdnean rodent Geor,vchus cupensis (Rodentia. Bathyergidac). Physio/. zool. 60: 174 180.

McNab, B. K. (1973). The rate of metabolism of the spiny rat Prowhimys .vaniispimsus, with comments on the ecological factors that influence the basal rate of metabolism in rodents and lagomorphs. B d . Aool. B d . Mor. (NS) 3 0 103.

McNab, B. K. (1979). The influence of body size on the energetics and distribution of fossorial and burrowing animals.

McNab, B. K . (1980). On estimating thermal conductances in endotherms. Physiol. Zool. 63: 1 4 5 ~ 156. Nevo, E. (1979). Adaptive convergence and divergence of subterranean mammals. A . Rev. Erol. Syst. 1 0 269-308. Nevo. E. & Shkolnik, A . (1974). Adaptive metabolic variation of chromosome forms in mole-rats, Spalux. E.rperientia 30:

Pearson, 0. P. (1947). The rate of metabolism of some small mammals. Ecology 2 8 127- 145. Vleck, D. (1979). The energy cost of burrowing by the pocket gopher Thomomys hotrae. Physrol. Zool. 5 2 122 136. Vleck, D. (1981). Burrow structure and foraging costs in the fossorial rodent, Thomomys bottae. Oecologia 49: 391 -396. Zar, J . H. (19x4). Biostatistical unalysi.7. Englewood Cliffs, New Jersey: Prentice Hall.

J . Zool., Lond. 220: 225 -248.

Cryptomys danrurt~n.sis (Rodcntia. Bathyergidae) 6 9 293- 302.

moles. S. A.fr. J . Zool. 2 3 189- 195.

mole-rats (Rodentia, Bathyergidae) in southern Africa. J . Arid Enrir. 22: 189- 198.

desert and mountain. Pliysiol. Zoo/. 47: 172 179.

Biochem. Phy.yiol. ( A ) 52: 35-38.

mammal? .I . T/zc,rtrw/ B i d . 16: 227-232.

open-circuit systems and in short-lag, closed-circuit apparatus. J . appl. Physiol. 10: 388- 392.

higdkri and Buthyerps maritimus. S . Afr. J . Sci. 5 4 293-302.

21: 283-288.

E d ( ) g y 60: 1010 ,1021.

124.~ 726.