J. Zool., Lond. (1994) 234, 477-487

The colony structure and reproductive biology of the afrotropical Mashona mole-r a t , Cryptomys darlingi

N. C. BENNETT, J . U. M. JARVIS Department of Zoology, Rondebosch 7700, Cape Town, South Africa

A N D F . P . D. COTTERILL Natural History Museum, PO Box 240, Bulawayo, Zimbabwe

(Accepted 19 November 1993)

(With 3 figures in the text)

Cryptomys darlingi occurs in the mesic Miombo woodland of north-eastem Zimbabwe. It occurs in colonies of up to nine individuals, in which reproduction is limited to one of the largest males and the largest female in the colony.

Reproduction and details of colony size and number of breeding animals in a colony are described for five complete field-captured colonies.

In captivity, mating is not confined to a particular season, and up to three litters of pups are orn per annum. The reproductive female initiates the pre-copulatory behaviour. The gestation lengt i is 56-61 days (n = 2). The new-born pups are altricial and litter size is small X = 1.7 0.5 (n = 6). In this case, the pups first left the nest 10 days after birth, began to eat solids when 14 days old, and were fully weaned at five weeks. They began to spar with each other when 36-40 days old, but did not disperse and were incorporated into the colony. This suggests that the Mashona mole-rat colonies are composed of a founding pair and at least three successive litters of pups.

Introduction . . . . Materials and methods Results . . . . . .

Colony structure . . Reproduction . .

Discussion. . . . . . Summary . . . . . . References.. . . . .

Contents

Page . . . . . . . . . . . . . . . . . . . . . . . . . . . . 471 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 480 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 483 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 485 . . . . . . . . . . . . . . . . . . . . . . . . . . . . 486

Introduction

The subterranean Mashona mole-rat, Cryptomys darlingi, lives in colonies of as many as nine individuals (Genelly, 1965; Bennett, Jarvis & Cotterill, 1993). It is herbivorous, feeding upon geophytes and underground swollen tubers (Genelly, 1965), which are encountered as the mole-rats burrow. Cryptomys darlingi occur in the mesic sub-tropical Miombo woodland areas of northern Zimbabwe (Smithers, 1983) and, until recently, it was considered a sub-species of Cryptomys hottentotus. However, details of its karyology show it to be a distinct species (Aguilar, 1993).

Published information pertaining to colony size is scant and details of the reproductive biology unknown (Smithers, 1983). In this paper, the colony structure and reproductive biology of the

477 0 1994 The Zoological Society of London

478 N. C. BENNETT ET A L

Mashona mole-rat is presented and compared with two other social cryptomids, namely, C. h. hottentotus and C. dumurensis. These three species all live in colonies in which there is a reproductive division of labour.

Materials and methods

Four colonies of mole-rats were captured at Goromonzi (173, 30"E) (2 in 1991 and 2 in 1992) and one colony in Harare (17"S, 31"E) (in 1987). The colonies were captured in the months June, July and August, 1987, 1991 and 1992.

The mole-rats were captured with modified Hickman live-traps (Hickman, 1979) or by cutting their retreat with a hoe when they came to seal opened sections of their burrow system (Jarvis & Sale, 1971). The mole-rats were captured over 4 consecutive days. If no animal came to the traps for 2 days after the capture of the last animal, the colony was considered trapped out. On capture, the mole-rats were sexed, weighed and their order of capture noted. The reproductive females were distinguished by their prominent axillary teats and the reproductive males by being the largest males in the colony.

In order to investigate reproduction and recruitment in the Mashona mole-rat, 2 pairs of reproductive animals were maintained in glass terraria. Wood shavings were placed in the tanks and paper towelling and dried grass were provided as nesting. Mole-rats were fed daily upon a variety of root and green vegetables, on apples, grapes and Pro-nutro@, a commercially-prepared balanced breakfast cereal. Food was given to the mole-rats daily, but they drank no free water.

The room temperature ranged between 26 and 28°C in summer and 20-23°C in winter. These temperatures are comparable to those recorded in the foraging burrows of other Cryptomys species (Bennett, Jarvis & Davies, 1988). During winter, a lamp placed next to the nest-box ensured that this was warmed to 25°C. The room was naturally lit from a window, however, when animals were being weighed or the cages were being cleaned, fluorescent lighting was switched on.

The animals were weighed weekly and growth curves were fitted with procedure AR of the BMDP (Biomedical Package) (Ralston, 1988), which fits non-linear regression models by an iterative least-square criterion. The Gompertz model for growth was chosen because it showed the lesser residual sum of squares. Using the Gompertz model, a growth rate and inflection point was obtained.

A growth rate constant (K = days-') allowed a comparison in growth amongst different species of Cryptomys. Individual maximum growth rates were determined by multiplying K by A.e-' (where A = asymptote and e = the exponential).

The mean maximum growth rate was obtained using the Gompertz equation:

W = A/xexp [-exp (-K x (t-ti))]

where W = predicted weight; A = asymptote; exp = exponential function; K = growth rate constant; t = age and ti = a parameter indicating the inflection time.

A complete colony of 9 mole-rats (Hl) containing a reproductive male and female were killed by anaesthesia using diethyl ether. The reproductive tracts were examined for signs of placental scars. The gonads were fixed in 5% formalin and prepared using standard eosin and haematoxylin staining technique (Drury & Wallington, 1967).

Results

Colony structure

Data from five colonies obtained at the time of capture are presented in Table I. The mean colony size was seven mole-rats (5-9 mole-rats) with a skew in the sex ratio towards males. The

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480 N . C . BENNETT ET A L

mean mass of adult males was 65.3 k 14.1 (n = 18) and females 62.9 14.9 (n = 15). The reproductive males in each colony were the heaviest animals in their colony, whilst reproductive females were nearly always the heaviest for their gender (Fig. 1, Table I).

There was little relation between body mass and the capture order of mole-rats (Hl), rs = + 0.53, (Gl), rs = - 0.40, (G2), rs = ~ 0.50, (G3), rs = - 0.27, (G4), rs = 0.30. Initial investigation by colony members to open or disturbed portions of the burrows was therefore not size-related (Fig. 1).

In the autopsied colony (Harare I), the reproductive female weighed 76 g and the reproductive male 84g. The uteri of the reproductive female were vascularized and had two embryos. Her ovaries were 5 mm long, granular in outline and contained two large corpora lutea. There were fewer unruptured luteinized follicles in comparison to the non-reproductive females. The uteri of the four non-reproductive females were thin-walled and bore no placental scars. The ovaries of these females were smooth in outline and had a length not exceeding 3mm. They contained primordial, primary and secondary follicles, in addition to many unruptured luteinized follicles.

The reproductive male and three non-reproductive males all showed evidence of spermato- genesis.

Reproduction

Courtship and copulation

In captivity, at the onset of reproductive activity in the reproductive female, the vagina became perforate. The reproductive female appeared restless and patrolled the burrow system more frequently than usual. On encountering the reproductive male, she would raise her tail and thrust her hindquarters into his face. Whilst doing this she emitted a deep guttural purr, and gently rapped her hindfeet on the floor. The male responded to this soliciting by pursuing her along the burrow system. During the chase both male and female vocalized, the former producing guttural purrs and the latter a twittering sound. Within a chamber the male pursued the female in a head- to-tail fashion. The male finally seized her tail with his incisors, mounted, held her around her shoulders with his forelimbs and bit her neck. The female responded by going into lordosis, whereupon the male released her neck and intromission proceeded. Thrusting was initially slow two thrusts/s reaching a peak of four thrusts/s prior to ejaculation.

Copulation was terminated by the female emitting a short squeal, whereupon the male dismounted. Mounting and copulation was completed within a minute. After copulation, the male autogroomed his genitalia. Multiple copulatory events were common, with several copulations taking place during one day.

Gestation

Copulations were observed on the 14, 15 and 18 November, 1992. The teats of the breeding female were swollen on the 16 November, and her body mass began to increase from the normal non-reproductive mass from 28 November, 1992. Two pups were born on 17 January, 1993 (Fig. 2). The estimated gestation period is therefore between 56-61 days. By the end of lactation, 44 days post-partum, the body mass of the female had dropped to 67g, 8% below her non- pregnant mass.

REPRODUCTIVE BIOLOGY OF THE MASHONA MOLE-RAT

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FIG. 1. Body mass, sex and order of capture of five colonies of Cryptomys durlingi. Female 0, Male @, Reproductive female 0, Reproductive male 0.

482 N . C . BENNETT ET A L .

-Gestation period=61 days --I

Parturition

90 88

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t/l

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Time (days)

F I G . 2 . Changes in body mass of a captive female Cryptomys durlingi prior to, during and after pregnancy. The gestation length is indicated by a horizontal bar.

Development of the young

New-born pups are 3 cm long, hairless and pink, except for purple pigmentation around the saddle and head. The coloration of the adult animal is already apparent with a clearly defined occipital head patch. The eyes and auditory meatus are closed, the digits of the feet are well formed and clawed and the extrabuccal incisors have erupted. If placed on their backs the pups can right themselves with difficulty. The pups produce high frequency cries. Pups at birth weigh between 6.9-8.2 g (n = 4). Offspring are unusually large and each individual may be 14% of the non-pregnant mass of the reproductive female.

The pups remain in the confines of the nest for up to 10 days after birth, during which they spent between 80-90% of the time resting and sucking. The pups suck from two pairs of axillary and one pair of inguinal nipples as the mother lies over them with her back arched. Sucking bouts are long, with babies remaining on the nipple for at least 30 min.

At day 4, the pups have a very fine pelage, with more hair distributed at the anterior end of the animal. By day 10 the pelage is silvery grey and the pups begin to wander from the nest. By day 12, the ear meatus is open.

At day 14, the eyes are partially open and the unweaned pups begin feeding upon solid food. The pups are agile and often leave the nest. They walk with their hind legs splayed out laterally. At day 19, the pups have a dark slate-grey pelage and the eyes are completely open.

By day 36, sibling-sibling interactions have become frequent, with sparring sessions occurring amongst litter mates and also their older brothers and sisters. At this stage, the pups are fully weaned, however, they do try to suck from the reproductive female. Her nipples decrease in size and by day 45 suckling has ceased.

REPRODUCTIVE BIOLOGY OF THE MASHONA MOLE-RAT 483

Litter size

Of the seven litters born to captive C. darlingi, five were of two pups and two were of one pup. 0.5 (n = 7). The time interval between litters for two

0 (n = 2). This was derived from the

The mean litter size born in captivity is 1.7 colonies were 112, 142 and 145 days.

number of pups captured wild and assuming no mortality. The mean litter size for field-captured colonies is 2

Growth rate

The mean growth rate for seven litters (seven male and five female pups) of C. darlingi from birth to 360 days old was 0.272 g per day. The increase in body mass follows the Gompertz model for growth (Fig. 3).

Discussion

The family Bathyergidae comprises five genera, three of which are solitary (Bathyergus, Georychus and Heliophobius) (Smithers, 1983; Bennett & Jarvis, 1988~). However, the family is set apart from all other subterranean rodents in having two social genera (Cryptomys and

W=92.614 exp(-exp(-0.008 (Age - 94.161))) 90

-10-

-20 , , 1 , , , , , , , , , , , 1 , , , , , , , , , , , , , , , , , , 1 I , , , ,

0 100 200 300 400

Age (days) FIG. 3. Generated Gompertz plot for postnatal body mass (9) against age (days) for six litters of Cryptomys darlingi.

Actual data points are represented by (a). A plot of calculated residuals for the Gompertz equation generated (0).

484 N . C . BENNETT ET A L .

Heterocephalus) characterized by a reproductive of labour and helpers at the nest (Jarvis, 1981; Bennett & Jarvis, 1988b; Bennett, 1989, 1990a, b; Burda, 1989; Jarvis & Bennett, 1993). Indeed, at least two species, Heterocephalus glaber (Jarvis, 198 1, 1985) and Cryptomys damarensis (Bennett & Jarvis, 1988b; Jarvis & Bennett, 1993) are eusocial.

Long-term field and laboratory studies on these eusocial bathyergids have shown that each colony contains a single reproductive female and 1-3 reproductive males. The remainder of the colony are typically their non-reproductive offspring, the majority of whom live a lifetime of socially-induced infertility (Bennett et al., 1993, 1994; Bennett, 1994). These non-breeders assist in the care of their younger siblings, in the finding of food and in defending the colony. The opportunity to breed only occurs on rare occasions when the animals disperse or, in the case of the naked mole-rat, when a reproductive dies. Colony numbers can reach 41 for the Damaraland mole-rat and 300 for the naked mole-rat, although in both species more usual colony sizes are about a third of these maxima.

Between the two extremes of sociality in the bathyergids (solitary-eusocial) lie a number of species of social Cryptomys. Although many details are still lacking, these cryptomyids show an interesting admixture of characteristics. Thus there are seasonal and aseasonal breeders, a range in mean body mass of 64 to 400 g, and some species occur in arid habitats while others inhabit mesic regions. The restriction of reproduction to a single female in the colony is a feature common to all cryptomyids studied to date (Bennett & Jarvis, 19883; Bennett, 1989; Burda, 1989), but in species breeding seasonally (C. h. hottentotus, C. h. natalensis) the male initiates courtship (Hickman, 1982; Bennett, 1989), whereas in aseasonal breeders (C. darlingi, C. damarensis, C. h.amatus, C. mechowi) it is the female (Bennett & Jarvis, 19883; Burda, 1989; Bennett, Jarvis & Cotterill, 1993; Burda & Kawalika, 1993).

Most cryptomyids have small litters (2-6 litters) (Bennett et al., 1991) and C. darlingi is at the bottom of this range (X = 1.7). This may account for the relatively small increase in the pregnant female body mass (24-31%) when compared with that of the slightly larger C. h. hottentotus (42%) whose mean litter size is three (Bennett, 1989). The relatively long gestation of C. darlingi of 56-61 days is comparable to that of most other bathyergids (Bennett et al., 1991). However, Burda (1989, 1990) has reported exceedingly long gestations (90-100 days) and lactation (77-88 days) for the Zambian species C. hottentotus (amatus) and C. mechowi. Burda attributes these prolonged pregnancies and suckling to the incapability of the reproductive female to store body fat and suggests that the evolution of eusociality in the Bathyergidae can be related to her need to have helpers at the nest to supply her with the nutrients she is unable to store as fat (Burda, 1990). Autopsy by us of freshly captured reproductive female C. h. hottentotus, C. darlingi, C. damarensis and C. h. amatus, as well as the solitary Georychus capensis, have failed to substantiate his claim. All of them stored fat and, in this, showed no obvious differences from the non-reproductives. Despite the long gestation, Cryptomys produce relatively altricial young whose mean maximum rate of growth and growth constants (K) are similar ( n = 3 species, Table 11).

Claims have been made that C. hottentotus (amatus) and C. mechowi from Zambia are eusocial (Burda, 1989; Burda & Kawalika, 1993). In these instances, observations on colony character- istics have been based almost entirely on captive animals. Only portions of colonies have been caught in the field (no reproductive females) and large colony sizes have been inferred from reports from local farmers and trappers. On-going field studies on C. h. hottentotus in the south- western Cape of South Africa (Rosenthal, Bennett, Spinks & Jarvis, unpubl.) have shown that colony structure in this species is more transient than in C. damarensis (Jarvis & Bennett, 1993),

REPRODUCTIVE BIOLOGY OF T H E MASHONA MOLE-RAT

TABLE I1 Themean growth rate constant ( K ) , maximumgrowth rate (K.A.e- ' ) , asymptotic weight ( A ) and inJIection time ( t i ) for the

Gompertz model calculated for three species of Cryptomys

485

Taxa A ti K K.A.e-'

Cryptomys darlingi 92.6 94.1 0,008 0.272 Bennett, Jarvis & Cotterill (this study) Cryptomys h. hottentotus 42.0 12.6 0,015 0.229 Bennett, Jarvis, Aguilar & McDaid (1991) Cryptomys damarensis 42.5 15.6 0.015 0-233 Bennett, Jarvis, Aguilar & McDaid (1991)

and that the majority of juveniles have left their natal colony before the next breeding season. The social structure in this species is therefore more similar to that of other cooperatively breeding birds and mammals (Emlen, 1982) and differs from the eusocial Damaraland and naked mole- rats. We therefore feel that until whole colonies are captured, and also the demography of wild populations is examined, the claims for eusociality in the Zambian cryptomyids, and indeed any other Cryptomys, are premature.

Despite the large gaps in our knowledge of the biology of many species of Cryptomys, enough is now known to indicate that this genus has the potential to offer invaluable insights into the interactions between habitat, resources, reproduction and colony organization in the Bathyergidae and the contribution of each to the evolution of eusociality in these mole-rats.

The family Bathyergidae is characterized by extended gestation periods most reminiscent of the Hystricidae (Bennett, 1989). It is unusual for mammals having long gestation periods and small litters to produce relatively altricial young, that are naked and helpless. The nidicolous condition of the young of all bathyergids may be a consequence of the thermally stable habitat of the burrow system. It is unlikely that extended periods of suckling has promoted sociality in the mole-rats as reported by Burda (1990) for C. h. amatus. It is of extreme interest that the mean colony size of C. h. hottentotus in temperate Africa is similar to that of C . darlingi in tropical mesic Africa. Yet the mean colony size of C . damarensis in xeric tropical Africa is markedly larger. This supports the aridity hypothesis as first proposed by Jarvis (1978) and further substantiated by Lovegrove (1987) and Bennett (1 988) which proposes that mole-rats occurring in environments with an unpredictable and low precipitation will promote temporarily larger colonies and increased cohesion and division of labour.

Further field studies investigating the temporal changes in the colony dynamics of C . darlingi will be particularly interesting, since recruitment to the colonies is unusually low. It is possible that, as in the common mole-rat, C . h. hottentotus, colonies are more transient in mesic areas where food resources are plentiful and rainfall patterns are more predictable.

Summary

Colonies of field-captured C . darlingi are composed of a reproductive pair and a number of non-reproductive animals. The reproductive pair are the largest by mass and linearly the longest. The colony size ranges from 5-9 mole-rats ( j t = 7).

Reproduction within captive colonies are described from the onset of courtship behaviour through to the incorporation of the young into the colony. The reproductive female mole-rat initiates courtship. Once the male and female meet, vocalizations and anogenital probing take place. Vocalization appears to be very important in courtship. Mating is brief but repeated many

486 N. C. BENNETT ET A L

times over the day. The gestation length is between 56 and 61 days and a litter of altricial young is born. Litters are small (1-2 pups) who are fully weaned at five weeks. The pups begin to feed on solids after 14 days. Inter-sibling sparring begins to develop at 36 days. The young mole-rats are incorporated into the colony and apparently ascertain positions within the dominance hierarchy by sibling-sibling and adult-sibling interactions.

These findings are compared and contrasted with other cryptomyids from southern and central Africa.

We thank Mr and Mrs A. Douie for permission to collect mole-rats on their farm in Goromonzi, Zimbabwe. We are grateful to the Chief Ecologist, Mr Drew Conybeare for his assistance and help in processing permits and in this light we also acknowledge the Department of National Parks and Wildlife Services for permission to trap and collect animals in Zimbabwe. We also thank Dr and Mrs C. Faulkes, Mr G. H. Aguilar, Mr N. Snow, Mr K. Schrumpf and Mrs P. Bell for assistance in the field work. This work was supported by grants from the University of Cape Town, and the Foundation for Research and Development (JUMJ and NCB). The field work was supported by a grant from the National Geographic Society.

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REPRODUCTIVE BIOLOGY OF T H E MASHONA MOLE-RAT 487

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