J. ZOO^., Land. (1996) 240, 221-231

The social structure and dominance hierarchy of the Mashona mole-rat, Cryptomys durlingi (Rodentia: Bathyergidae) from Zimbabwe

U. GABATHULER', N. C . BEN NETT^^ A N D J . U. M . J A R V I S ~

'Dqmrtinent qf Zoology, University of Zurich, Zurich, Switzerland; 2Depurtment of' Zoolog?!, University of Cape Town, Rondehosch 7700, South Ajrica

(Accepted 6 July 1995)

(With 2 figures in the text)

C r y p t c m j . ~ dudingi is a social subterranean rodent mole which inhabits the mesic regions of south-eastern and central Africa. Mashona mole-rats live in small colonies (5-9 animals) in which reproduction is normally restricted to the largest male and female in the colony. The non- reproductive members in a mature colony cannot be placed into clearly defined work-related groups based on body mass.

The dominance hierarchy of a young colony was found to be linear, with a value of 1.00 calculated from Landau's linearity index. while that of a mature colony of nine mole-rats was almost linear (0.77). Dominance was found to be related to gender in the mature colony, with males more dominant than females, and to age in the young colony. The reproductive mole-rats are the dominant animals within their respective genders. Dominance appears to correlate positively with body mass (rs = 0.77 in the mature colony and rs = 0.93 in the young colony).

Popularity studies show that smaller animals and females tend to be more popular than the larger massed individuals or males. In the mature colony which contained predominantly adult animals, the reproductive pair was among the least popular. While in the young colony. composed predominantly of suh-adult and juvenile animals, the reproductive pair was the most popular.

Social organization within Mashona mole-rat colonies is compared with other southern African Crjytomys species.

Introduction

The Mashona mole-rat, Cryptomys durlingi occurs predominantly in the mesic Miombo woodlands of north-eastern Zimbabwe and southern Mozambique (Skinner & Smithers, 1990). It is a subterranean rodent occurring in large burrow systems which ramify through the soil forming an intricate labyrinth. Colony size ranges from 5-9 individuals in which reproduc- tion is restricted to the largest male and female in the colony (Bennett, Jarvis & Cotterill, 1994). Recruitment to colonies is low (two pups per litter), and this could in part be responsible for the numerically small colonies (Bennett, Jarvis & Cotterill, 1994). The mole-rats grow slowly, which may be partly due to the poikilothermic thermal characteristics of the mole-rat (Bennett, Jarvis & Cotterill, 1993).

Recent qualitative and quantitative studies on a closely related species, Cryptomys hutrmzurus, which occupies mesic sub-tropical environments in South Africa, have supported the idea of this loosely social mole-rat having a poorly defined work-related group. The present study examines

'Present address and address for correspondence: Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa

221 #C3 1996 The Zoological Society of London

'.-- 777

the social s t ructure of captive colonies o f C. rlurliyqi in relation t o dominance/subordinance relationships a n d in relation t o 'work' (here defined as activities deployed by the mole-rats in finding food and maintaining the bur row system).

To date , the eusocial D a m a r a l a n d mole-rat which occurs in the tropical arid rcgions of central and southern Africa is the only mole-rat found t o have a strongly linear hierarchy in which the non-reproductive caste can be fur ther divided into two worker groups based on body mass (Bennett & Jarvis. 1988: Jacobs c't ~11 . . 1991).

This study is iniportant i n that i t investigates the degree of sociality in a mole-rat which is found in a mesic tropical environment and yet it breeds aseasonally. The sociality of this mole-rat is compared with that o f an arid tropical aseasonally breeding mole-rat (C~:,ptomys u'lirnarmsis) and a niesic sub-tropical mole-rat which breeds seasonally (C. 11 . ltortm/otm) (Bennett & Jarvis, 1988; Bennett. 1989; Jacobs rr d.. 1991).

U G A B A T H U L E R . N . C. B E N N E T T & J . U . M . J A R V l S

Materials and methods

One complete colon) (Colony A). consisting of 9 mole-rats, was captured at Goromonzi ( 1 7 S, 31 'E)- near Harare, Zimbabwe in June 1997. A second colony (Colony B). containing 7 mole-rats, was initially formed by a pair of mole-rats from 2 different colonies that had been captured at Goromonzi, in July 1990. This pair gave birth in captivity to 5 animals from 3 litters. The mole-rats were captured with Hickman live- traps (Hickman. 1979). or by cutting off their retreat with a hoe when they come to seal opened sections of their burrow system (Jarvis & Sale. 1971 ). On capture. the mole-rats were toe-clipped ( to enable long-term identification), sexed. and weighed. A licence to toc-clip the mole-rats was authorized by the animal ethics committee of the University of Cape Town.

In November 1997. Colony A was housed in a system of transparent Perspex tunnels (65mm x 60nim x hSrnni) linking 4 transparent chambers which served a s a nest. food stores, and a toilet area. Colony B was subsequently housed in the samc system in February 1993. Two digging areas consisting of 6 parallel burrows of 0.5 m were given i n which the molc-rats could excavate sand from the base of the arena and kick i t along the tube to a a.irc mesh grid where it fell through into a collecting bucket. Tissue paper was supplied its nesting material and wood shavings were placed in the chambers. The toilet area was cleaned daily and the entire system weekly.

The room temperature ranged between 26 C and 28 C and the relative humidity of the room was maintained at 50%, (Bennett. Jarvis & Davies. 1988). The room \vas illuminated with constant light during the observation period.

C ' r ~ j p o n z w dm/i/rgi have small cyes which they keep closed except when alarmed. In the colonies under observation. no obvious behavioural response was detected to bright flashes of light or to movement by an observer. a s long as i t was not accompanied by sound or by iin air current. It was therefore assumed that, in this study. the behaviour ofanirnals was not disturbed by thc artificial lighting. It was not possible to assess the extent to which captivit! affected the colony behaviour. Detailed field observation of behaviour of animals that live completely underground are not possible.

The mole-rats werc fed on a variety of chopped fruits. roots. and green vegetables. The food was placed cither in the food chambers or buried in the sand of the digging areas where i t could be obtained as the mole- rats euca\iited thc sand. The mole-rats drank no free Lvater and obtained a positive water balance from the food source.

The white occipital head patches of the mole-rats were marked with a number of non-toxic dyes. The dye- code. together with their variation i n body sire. rendered individuals easily distinguishable from one another.

The roles of the individuals within the colony were established from l20h of observation in Colony A and 70 ti in Colon> B. For 90'4) of the time. at least half of the mole-rats were inactive within the

SOCIAL STRUCTURE OF MOLE-RAT 223

nest and it was therefore possible to record all the behaviour of the active colony members. The observation periods ranged between 1 h and 12 h and were spread over the 24-h period of the day. The data were collected by scan sampling (Altmann, 1974) in which the behavioural acts of the animals were recorded every minute and entered on to prepared sheets by a written code. If there were any disturbances to the colony (external noises), the observation session was terminated for a t least an hour to allow the colony to settle down.

A dominance index, D.I. (Aspey, 1977), was constructed to establish whether a dominance hierarchy existed in the colony. The dominance hierarchies were determined from 20 h of observation in Colony A and 10 h in colony B. The dominance index was calculated using several parameters: the behaviour type. its intensity weighting and the frequency with which that interaction occurred between each individual in the colony. Interactive behaviours were subjectively allotted an intensity weighting (an arbitrary scale of -5 (passive) to +5 (aggressive) interaction) based on their grouping by the previous R-type factor analysis (Aspey, 1977).

” Behavioural frequency x Intensity weight D.I. =

Total number of interactions I

The following behaviours were recorded: biting, tail-pulling, threatening, shunt-flicking, ramming. stealing food successfully, reverse ramming, chasing, pulling, sparring, passing over, passing side, allo- grooming, passing under, being blocked, retreating, unsuccessful attempt to steal food and vocalized hopping. A detailed ethogram explaining these behaviours can be found in Jacobs et al. (1991) and Rosenthal, Bennett & Jarvis (1992).

Using the D.I., the number of individuals over which each animal was dominant, its dominance value (D.V.), and subordinate (S.V.), were determined.

The presence of a dominance hierarchy and its linearity were tested using Landau’s index of the strength of a hierarchy (Bekoff, 1977), which separates strong linear hierarchies from non-linear hierarchies.

Where n = number of animals in the group and Va = number of individuals that an animal dominates. The term 12/(n’-n) normalizes h, so that the value ranges from 0 to 1. When h = 1, the hierarchy is linear. Conversely, when h = 0, each animal dominates an equal number of group members. An h value > 0.9 was used as a cut-off for separating strong linear hierarchies from others (Chase, 1974).

Popularity was quantified as the number of interactions received subtracted from the number of interactions initiated (Rasa, 1977).

Results

Colony composition

Colony A was completely wild captured and consisted of nine mole-rats (four males and five females). The animals ranged in mass from 49.5 to 109.3 g (Table I). Colony B was composed of seven mole-rats which ranged in mass from 24 to 103 g (Table I).

Based on their reproductive role, the members of colony A were divided into two castes (Fig. la). The reproductive caste was composed of two breeding animals (M1 and F2). The breeders were the heaviest and largest animals in their respective gender. Between 7.9 and 12.2% of the total burrow maintenance work performed by the colony was done by the reproductives. The non-reproductive caste performed between 4.5 and 20.4% of the total colony work (Table 11). Two groupings could be discerned amongst the non-reproductives, those performing between

2'4 U . GABATHIJI -ER. N . C . B E N N E T T & J . U . M . J A R V I S

TABLE I ~ i ~ r I f p i i . \ i / i o t i of fit'u Cryptonlys darlingi r~i/otiir.\

No. of Sex N o . oS Mean body No. of Mean body Mean body Colony animals ratio males mass males (g) females mass females (g) mass all (8) Biomass

Col. A 9 0.x I 71.63 (+26.11) 5 60.76 (k13.54) 53.4 (f12.33) 480.7 Col. B 7 0.75 3 83.00 (k20.00) 4 46.25 ( f23 .13 ) 62.0 (128.04) 434.0 Total 16 7 76.50 (f22.61) 9 54.31 (rt18.73) 57.17 (120.37)

____ -____._ - -~

12.4 and 20.4% of the total work 'frequent workers'. and those performing between 4.5 and 8.8% of the total work 'casual workers' (Table 11). The three categories did not differ significantly in the body inass of the respective members Kruskal- Wallis test H = 4.0, P = 0.135, N.S. Similarly, there was no statistically significant difference in work frequency with cex.

The members of colony B comprised the founding reproductive male (M10) and the reproductive female (F1 I ) . The largest non-reproductive member (M 12) worked less (10.1 YO) than the two lighter animals (M13, F14) born three months later (18.8 and 19.7%). The two smallest colony members (Fl5 and F16) worked the least, perhaps because they were juveniles and not large enough to work (Table 111) and Fig. 1 b.

In general. mole-rats In colony A performed work-type behaviour about half as much as colony €3 (X = 3.0 t 1.5 h- ' , and 6.1 + 7.0 h-l. respectively).

Doniiiuirtce iiidev

Each behaviour involving an interaction between two animals was subjectively allotted an intensity weight which ranged from -5 (very submissive) to f 5 (very aggressive). The various behaviours involving an interaction between two animals and their intensity weights are presented in Table IV and dominance indices in Tables V and VI.

Weight Work Work D.I. Rest I nd Group (g)* (fr h) (%) ( 1

~

M I 1-2 M3 M4 'Mi

t 6 t 7 F8 F9

~~

repr . repr. C . W .

C.W.

c.w. C.\V

t: w . S.W.

I: \v .

109.3 (13.5) 73.4 (i4.3) 66.8 (14.5) 6O.X ( i 3 . 3 ) 49.6 (13 .7) 77.5 (15.3) 50.3 ( 3 2 6 ) 53.0 ( 1 3 . 5 ) 49.5 (k2.6)

3.92 2.13 1.74 1.27 1.37 7.20 5.23 3.34 5.51

12.2 7.9 6.4 4.5 8.8 8. I

12.4 19.4 20.4

8 6 6 5 2 4 2 1 7 &

77.5 80.1 80.1 83.9 75.9 79.9 78.8 77.2 77.3

*The hod! masses are the nican inasses of the animals. measured during the observation period Gt-oitp. repr.. 'reproductives': c . ~ . . 'casual workers': f.14.. 'frequcnt workers'

SOCIAL STRUCTURE OF MOLE-RAT

16-

8 14- h

v g 12:

10 -

235

‘ Q

(b) Colony B 20

18 - d

8 : 6 9

I I I 1

?

CT

!O Mass (9)

F I G . 1. (a) The percentage of the total burrow maintenance activity performed by the nine mole-rats in colony A as a function of body mass (8). Shaded circles represent the reproductive animals. (b) The percentage of the total burrow maintenance activity performed by the seven mole-rats in colony B as a function of body mass (g). Shaded circles represent the reproductive animals.

Colony A

The most dominant animal in colony A was the reproductive male M 1. The reproductive male (Ml) and reproductive female (F2) were the most dominant animals in each respective gender. The next most dominant mole-rats were the heavier males (M3 and M4) and the heaviest female (F6) was ranked fifth in the colony. The four smallest animals were the most subordinate (M5, F7, F8, and F9) (Table V).

The most dominant mole-rat in colony B was the reproductive male M10 followed by the reproductive female (F1 1). The reproductive animals were the most dominant animals in the respective genders. The two larger non-reproductive mole-rats (M 12 and F14) were dominant, whereas the three younger mole-rats (M 13, F15, and F16) were subordinate (Table VI).

376 Li. G A B A T H U L E R . N . C . B E N N E T T & J . U. M . J A R V I S

T ~ H L ~ 111 Tlw hoili. ni(i.\.\, ~~~ork,f~rqurric:, . . i/oniinancc~ i n d ~ ~ , atid re.siinfi,fi.e~jiirtic~. of'niolr-rais in colony B

Age Weight Work Work Rest Ind. (month\) @)* (fr. h) 1 D.I. (YO)

- ~ ~~ .~

M 10 repr. 103 7.5 17.4 6 64.9 FI I repr 70 6.6 15.3 5 69.8 M I 3 10 83 4.3 10.1 4 63.9 M I 3 7 63 8.1 18.8 2 60.7 F14 , 67 8.5 19.7 3 58.1 FIS 29 4.6 10.7 1 65.8 F16 24 3.4 8.0 0 75.4

1

7

*The bod! masses o f the animals in colony R were taken at the beginning of the observation period

Behavioural acts

Biting. tail-pulling Threatening, shunt flicking Ramming. stealing food successfully Reverse ramming. chasing, pushing Sparring, passing over p. cissing : side. allogrooming Passing under. being blocked, retreating Unsuccessful attempt to steal food Vocalized hopping

I nitkiton:

M1 F2 M3 M4 M 5 F 6 F7 FX F9 D.V. s v. Ranking

~. ~

MI - -

+0.98 + I .98 t1.27 -1.94 j 1.40 i 1.73 +1.70

I 1.44 8 0 D

F3

-0 89 - -

-0 1 1 - 1.42 -1.97 -2.15 -1.53 - 1.56 c1.32

6 - D

M 3 M4 MS

- 1.68 +0.64

+ 1.42

+ 1.27 + 1.46 -0.91

1-7.07

+OX2 6 - D

-2.10 -0.18 -1.08

T 1.33 0000 +1.08 t1.10 11.55

5 3 D

~

-2.03 - I .68 +2.33 - I .87

+0.30 -0.39 +0. 19 t0.56

2 6 S

-

F6

-2.25 -3.37 -2.28 -1.56 + 1.56

t0.86 +0.57 +1.20

4 4

-

F7

-0.33 - I .46 -1.50 -6.60 t1.10 -2.00

__ -

+0.79 -0.58

2 6 S

F8 F9 - -

-0.69 -0.31 -1.72 -2.45 -0.76 -1.70 0000 -0.08

+0.88 -0.27 -1.70 -0.67 -0.63 +0.94 - +0.19

-0.22 -

1 2 7 6 S S

Bold = Illitrator dominate, receker D.V. L Dominance value; D = dominant animal S.V. = Subordinance vuluc: S - subordinate animal The dominance indices for all mole-rats (column) with ebery other mole-rat (rows) were used to determine (D.V.)

Rankiiiy \ h o w i-elatne dominance arid subordinance allocation to each colony member. dominance and (S .V. ) subordinance values.

SOCIAL S T R U C T U R E O F M O L E - R A T 227

TABLF, V1 Dornincmce indice.y,for each individual (columns) with every other individual jroiosj ,for the seve~z rnriiiher~ of colori~ B

Initiators: M 10 F1 I M I 2 MI3 F14 F15 F16 ~~

MI0 FI 1 MI2 M I 3 F14 F15 F16 D.V. S.V. Ranking

~~

+0.81 +1.71 +2.03 +1.44 +1.60 + 1.66

6 0 D

+0.68

f1.34 + 1.04 +1.50 +1.60 +0.20

5 1 D

- +0.81 +1.11

+0.97 +1.17 + L O O +1.25 4 2 D

~~

-0.35 -0.61 -0.13 -

f0.95 +1.38 +0.82

2 4 S

- 1.76 -2.41 -0.38 f1.30

+Oh3 +0.90

3 3

-

-

0000 -3.00 -2.40 -2.20 -3.67 -

+0.96 1 5 S

- 1 .OO -0.33 -0.50 - 1.33 -0.66 +0.74

n 6 s

Bold = Initiator dominates receiver D.V. = Dominance value; D = dominant animal S.V. = Subordinance value; S = subordinate animal The dominance indices for all mole-rats (column) with every other mole-rat (rows) were used to determine (D.V.)

Ranking shows relative dominance and subordinance allocation to each colony member. dominance and (S.V.) subordinance values.

In both colonies there was found to be a strong correlation between dominance ranking and body mass (Colony A, rs = 0.77 and Colony B, rs = 0.93 ), respectively.

Linearity qf the hierarchy

The index of the dominance linearity (h) for the nine mole-rats in the mature colony (Colony A) was 0.77, whereas in the young colony (Colony B) it was 1 .OO.

Popularity study

Popularity was negatively correlated with body mass in colony A (r, = -0.78) and in colony B (r, = -0.35) (Figs 2a and b). However, while popularity was still negatively correlated with dominance position in colony A (r, = -0.46), no such relationship was found in colony B

Mole-rats in colony A sparred far less frequently than individuals in colony B. Similarly, individuals in the younger colony tended to perform work activities far more frequently than those individuals occurring in the mature colony (Table VII). Many of the more aggessive activities were performed with equal frequency amongst members of the two colonies (Table VII).

(rs = 0).

Discussion

Over the last decade an increasingly substantial body of evidence has accumulated, linking the degree of sociality in the Bathyergidae with two ecological factors: aridity and the distribution of food. This has led to the aptly termed ‘food aridity hypothesis’ (Jarvis, 1978; Lovegrove & Wissel, 1988) in which it is postulated that the degree of sociality exhibited by the mole-rats is related to the size and clumping of the food resource and the rainfall.

72s C G A B A T H L L F R N C B E N N E T T S r J U M J A R V I S :

F I C , 2 . ( : I ) Ihr popularit) (nunihei- of interactions receiwd subtracted from the number of interactions initiated) of tach mole-i.ar in colony A with respect to otlier mcmbers. (h) The popularity (number of interactions received subtracted ltom the nunibrr of intei-aciionh initiated) of each mole-rat in colony B wilh respect to other members.

Of all the hathyergid genera. Crjp ton~ j~ .~ has the widest geographic distribution and contains the largest number of species. All species of CrJptomj's studied so far, characteristically have reproduction restricted to a single female and usually one male (Bennett & Jarvis, 1988; Bennett, 1989; Burda. 1989: Burda & Kawalika. 1993; Bennett, Jarvis & Cotterill, 1994). Delayed dispersal

SOCIAL STRUCTURE OF MOLE-RAT 229

TABLE VII The frequencies of behavioural acts in both colonies of Cryptornj Y darlzngi

‘Fighting elements’ ‘Work’ __-__ Behdviour ‘Sparring’

elements 1 2 3 4 5 6 I 8 9 ____ _- -~ __ --______

Colony A (frequency/h) 1.8 6.3 2.4 3.7 1.8 4.5 1 .0 18.0 2.9

Colony B (frequency/h) 31.0 1.3 3.9 2.4 0.2 3.3 1 .o 38.2 4.9

Behaviour elements: 1: sparring 2: stealing food successfully 8: digging

3: tail-pulling 9: transporting 4: biting 5: threatening 6: ramming 7: shunt flicking

The behavioural interactive and burrow maintenance elements recorded in the two colonies of Cryp/om,v.s dar/ifzgi. The corresponding number refers to the behavioural type recorded in each of the colonies.

of offspring leads to the formation of a colony workforce of non-reproductives. Species of Cryptomys occur in mesic and arid habitats in the tropics and more temperate regions, and the degree of sociality ranges from pairs (Cryptomys hottentotus natalensis) (Hickman, 1982), through species occurring in small colonies such as Cryptomys hottentotus hottenrotus (Bennett, 1989) and C. darlingi (Bennett, Jarvis & Cotterill, 1994) to the eusocial Crjptomys damarensis (Bennett & Jarvis, 1988, Bennett, 1990; Jacobs et al., 1991).

Long-term studies on the population dynamics of C. damarensis (Jarvis & Bennett, 1993) and C. h. hottentotus (Spinks & Bennett, In prep.), as well as field and laboratory studies on these and other species of Cryptomys, are providing an increasingly comprehensive database on which to test and refine the food-aridity hypothesis. There are, however, still many gaps in our knowledge. Our study on C. darlingi addresses one of these gaps.

Cryptomys darlingi is of interest in that it occurs in mesic regions of Zimbabwe, where, according to the food-aridity hypothesis, there should be fewer ecological pressures promoting sociality, and animals should either be solitary or live in small colonies of a transient nature. It also provides a tropical example that can be compared with the mesic species (C. h. natalensis and C. h. hottentotus) occurring in the more temperate parts of South Africa where seasonal temperature extremes are more variable.

Many of the differences found between the Mashona mole-rat C. darlingi, the common mole-rat C. h. hottentotus, and the Damaraland mole-rat C. damarensis are ones of detail rather than magnitude. In all three, the dominance organization was similar, with the reproductive male at the apex of the hierarchy followed by the reproductive female, and the non-reproductive males being dominant to the non-reproductive females (Bennett, 1989; Jacobs et al., 1991; this study). A linear hierarchy, normally indicative of a stable social system, is present in all, but more strongly evidenced in mature, colonies of C. dainarensis than in C. lz. hottentotus and C. darlingi, whose colony sizes are also smaller. These latter two factors may indicate that mole-rats occurring in the mesic environ- ments have colonies that are less organized and more transient (dispersal events occurring on a more regular basis than in arid regions). If so, this would lend support to the food-aridity hypothesis.

230 U . GABATHULER, N . C . BENNETT & J . U. M. JARVIS

Within the invertebrates and vertebrates is found a spectrum of social organization-many species of which exhibit all the criteria for eusociality (Michener, 1969; Wilson, 1971) namely: i) a reproductive division of labour; ii) co-operative care of the young; iii) an overlap of at least two generations. They, however, vary in the strength and duration of the 'reproductive division of labour'. Sherman rr nl. (In press) propose a simple quantitative means of comparing the social systems of co-operatively breeding species in which the probability of an individual in a social group ever breeding, or its 'lifetime reproductive success', is used to define the degree of reproductive division of labour. In the Damaraland mole-rat, field studies (Jarvis & Bennett, 1993) have shown that ecological constraints limit opportunities for dispersion, and about 90% of all non-reproductives in colonies live a lifetime of socially-induced sterility (Bennett et al., 1993, 1994). Comparable field data are unavailable for the mesic species but we should predict from their small colony numbers and less stable colony organization that opportunities for dispersal and of becoming reproductives in new colonies are greater for these species.

A study on the colony dynamics, population biology, and colony ergonomics in the field will shed further light on mortality, colony turnover, and dispersal patterns in this underground forager in Africa.

We thank M r and Mrs A. Douie for permission to trap mole-rats on their farm in Goromonzi, Zimbabwe. The Department of National Parks and Wildlife Services are thanked for providing the necessary collection permits. Dr and Mrs C. G. Faulkes, Mr G. Aguilar, Mr N. Snow, Mr K. Schrumpf and Mrs P. Bell are thanked for help in collecting the mole-rats. This work was supported by a National Geographic travel grant to (JUMJ) and research grants from the University of Cape Town and Foundation for Research and Development (to NCB and JUMJ).

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