Laboratory Animals (1992) 26, 88-99


Sex ratio and mortality in a laboratory col()inyof the common marmoset (Callithrix jacchus) HARTMUT ROTHE, KURT DARMS & ANDREAS KOENIG Institute of Anthropology,

University of Goettingen, 3400 Goettingen, Buergerstrasse 50, Germany

Summary In a retrospective study sex ratio and mortality were analysed in a captive colony of common marmosets (Callithrix jacchus). Seven hundred and thirty-five infants in 294 litters (20 singletons, 119 twins, 140 triplets, 14 quadruplets) out of 57 breeding females were evaluated. The sex ratio at birth was O· 95 males: 1· 0 females. The frequency of males and females, as well as the sex composition of twins and triplets confirm the assumption of dizygotic twinning in the common marmoset. According to age at death, 9 categories were differentiated, with perinatal mortality being the highest. Once early infancy had passed the probability of a common marmoset infant of our colony reaching childhood is nearly 95070. Sixty per cent of all liveborn infants survived beyond 18 months. Morta1ity of infants at birth from primiparous mothers did not differ from that of pluriparous females, nor did the survival rate of infants with the filial generation the respective female had reached (F 1 to F6). Females with a high ratio of triplets and quadruplets had a lower reproductive success than females with a majority of singleton or twin deliveries. Differential mortality between males and females was not observed. The frequency of stillbirths was not strongly related to parity, but was to litter-size. Most stillborn babies were seen· in sets of quadruplets, most abortions in singletons. A normal socialization in a stable social environment, as well as not pairing the animals before they are fully adult, are considered important factors in good breeding success and infant survival. Received 17 December 1990; accepted 13 July 1991

Keywords: Sex ratio; Infant mortality; Perinatal mortality; Longterm study; Common marmoset; Callithrix jacchu> The marmoset colony of the Institute of Anthropology, University of Goettingen, started in 1968 (at the Institute of Anthropology, University of Kid) with 2 mature males and 2 females importd from Recife, Pernambuco, Brazil. From 1%8 through 1990, 63 pairs were formed to which a total of 735 infants were born. The colony size was limited to about 100-120 animals, Le. approximately 12-15 social units. Supernumerary animals, which were not used for breeding or ethclogical studies, were regularly loaned to different institutions, including zoos, for breeding. Except for 3 males and 2 females which had been imported illegally and which were confiscatec. by the German customs and given on a bre,~ding loan agreement to our institute, recruitment of genetically unrelated specimens (n = :12) was done exclusively by exchange trade with other institutions (e.g. zoos, universities, etc.), or on a breeding loan agreement. Hence, (,ur marmoset colony has not exploited the natural resources for more than 20 years. This study is retrospective and examines the sex and mortalit~, ratio of parent-reared common marmosets bon in our colony from 1968 through 1990. Materials and methods The animals were housed indoors in wire mesh cages or rooms I)f 2· 0 m3 to 73, 5 m3• The great majority of the pairs/families had no physical

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Sex ratio and mortality in the common marmoset or visual contact with each other; however, acoustic and olfactory contact via central air conditioning probably occurred. The cages and rooms were equipped with free swinging as well as fixed climbing branches, one to 4 feeding boards and one to 4 sleeping boxes. In addition to natural light, artificial lighting was provided by neon bulbs on a 12-h cycle (6 a.m. to 6 p.m.). A constant temperature of 25°C to 27°C and a relative humidity of about 700/0were maintained by means of an air conditioning system. Cages and rooms were cleaned daily and disinfected twice a week [until 1989 with Sagrotan, SchUlke & Mayr Company, then until 1990 with Labo AId, Deppe Company, and from 1990 to date (July 1991) with Septanin Plus, Schur Company]. The animals were fed twice daily. In the morning they were provided with a mixture of boiled rice and oats which was supplemented with skimmed milk powder, curd, mashed beef, yeast, liver meal, sunflower oil, wheat germ oil, lemon juice, minerals and vitamins. In the afternoon they were fed a mixture of sliced fruit (apples, bananas, oranges, raisins), vegetables (cucumbers, carrots, tomatoes), and hard boiled eggs. A commercial diet (for cats) containing a high ratio of taurine was offered twice weekly. Baby mice and mealworms were offered for many years, 3 times per week but have been subsequently replaced by crickets. Unsweetened black tea was provided ad libitum. All animals were irradiated with ultraviolet light (UV A) for 3 min twice a week. Infants were left with the parents until they were expelled from the family (Rothe et al., 1986). We did not manipulate the demographic structure of the social units unless it was necessary due to the loss of one or both parents, or to a subsequent splitting up or even dissolution of the group due to a specific research project (for details see Koenig et al., 1988). Except for one pair (hand-reared in a peergroup), all remaining breeding females and males had infant-rearing experience and, except for a very few cases, all males and females which were paired, were at least 18 months old.

89 Records of all common marmosets born during a 22-year period from 1968 through 1990 were reviewed. Data on litter size, litter composition, sex of infants, generation and parity of the mother were collected for analysis. According to the age at death of infants 9 categories were differentiated: Category 1: abortions (birth of not fully developed embryos/fetuses), premature deliveries (birth of fully developed, but not fullterm infants weighing less than 26 g), stillborn (infants still enclosed in the fetal membranes; additionally, infants found dead and still connected to the expelled but otherwise untouched placenta; autopsy of 4 of these infants revealed no inflation of the lungs; the placenta and the umbilical cord of these infants were never eaten by the mother and/or other group members; we therefore considered all these infants as stillborn, keeping in mind that this classification was not correct in any case) or animals found dead (umbilical cord was cut and placenta eaten) and for whom there was no knowledge of whether they had breathed; Category 2: animals which died or were killed by the parents or siblings within the first day; Category 3: included live born that died within days 2 to 7 (mortality until day 3 is defined here as perinatal mortality); Category 4: animals which died between days 8 and 30 (approximate age when regular carrying of infant drops substantially); Category 5: animals which died between days 31 and 90 (approximate age when mother terminates lactation); Category 6: death between days 91 and 150 (age when the next litter is likely to be born; mortality until day 150 is defined here as infant mortality); Category 7: animals which died between days 151and 365 (subadulthood); Category 8: death between days 366 and 547 (adulthood); Category 9: animals which died beyond day 547. Non-viable or incurable infants/animals were humanely killed. Post mortem examination was performed with all animals older than 2 weeks, whereas younger infants/animals were only examined when starvation could not be excluded as first order cause of death (seealso p. 97). The autopsy data willbe published elsewhere (Brack & Rothe, in preparation).

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Rothe, Darms & Koenig Table 1. Litter-size, litter-composition and sex ratio






Singletons n=20 (6'8070) Twins

8 40,0 105

9 45·0 123

3 15·0 10

20 100,0 238

n= 119 (40'5070) Triplets

44·1 197

51·7 197

4·2 26

100,0 420

n= 140 (47'6070)










n= 14 (4,8070)





Unknown n= 1(0'3%) Total n=294

I 100,0 335

354 48·2


46 6'3

Litter composition

mm: 24 mf: 57 mmm: 16 fff: 12 mmf: 42 mff: 54 mmmm: I ffff: I mmff: 4 mmmf: 2

ff: 31 fu: 4 mmu: muu: mfu: ffu: mfff: mffu: mmfu: ffuu:

2 2 5 3 2 I I I

uu: 3 uuu: 4

muuu: 1

1 100,0 735 100'0

f = female; m = male; u = unsexed.

On 4 occasions we detected blood on the cage floor. Since none of the group members showed any wound, we tentatively considered these events as early abortions but we did not include them in the analysis, since we could not be completely certain whether the respective breeding female had aborted or not. Finally, the first litter of one female consisted of hybrids (c. jacchus X C. penicillata) and was thus not evaluated, although taken into consideration when calculating the parity of the respective female. The breeding females of our colony had differing numbers of litters (see Table 3a), depending partly on the age of the respective female or on the duration of the groups' existence and partly on the duration of its membership in our colony. See Table 3b for the generation of the breeding females. Chi2-test, Cramer's coefficient (Siegel & Castellan, 1988)and z-test (Haseloff & Hoffmann, 1968) were used for statistical analysis of the data.

litters (20 singletons, 119 sets of twins, 140 sets of triplets, 14 sers of quadruplets, one unknown) from 57 breeding females (9 wild-born, 48 captive-born) of 63 groups could be analysed. Fifteen females gave birth to I to 5 infants, 12 females to 6 to 10, 13 females to 11 to 15, 4 females to 16 te· 20, 11 females to 21 to 30, one female had 31 :.nfants and finally, one had 44 infants. Except for one female (4 male infants, 18 female infants; x2=4'5, df= 1, P0'05; n = 112. tMales versus females: X2=0'0; df=3; P>0'05; n= 124.


12 54 42

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Sex ratio and mortality in the common marmoset



stillborn = 7,9 % (n= 55 fullterm: n= 3 premature) male= 25: female= 23: unsexed= 10 aborted = 2.6 % (n= 19)


male= 7: female= 0; unsexed= 12 live-born = 89,5 % (n= 654 fullterm; n= 4 premature) male= 304; lemale= 331; unsexed= 23

Fig. 1. Absolute and relative frequency of live-born, aborted,


and stillborn infants.

of males (48' 62070)and females (51' 38070)from the 1 : 1 sex-ratio is not significant for the total number of males and females born in our colony (x2=0'26, df= 1, P>0'05) as well as for the number of live-born males and females (x2=0'62, df= I, P>0·05).

The most frequent number of offspring was 3 (47-6070),followed by 2 (40-5070),one (6'8070) and four (4 -8070)(Table 1; see also Rothe et aI., 1987). The distribution of the different twin and triplet litters (quadruplets could not be evaluated due to the limited number) and the differences between observed and expected frequency, (assuming a P = O' 5 = male frequency = female frequency) is shown in Table 2. The total number of males (n = 335; n = 303 live-born) and females (n = 354; n = 331 live-born), the distribution of uni- and heterosexual litters [approximately one (unisexual male) : 2(heterosexual male/female) : one (unisexual female)], as well as the frequency of males and females in the different twin- and triplet litters,(twins: x2=0'44, df=2, P>0'05; triplets: X2=0'0, df=2, P>0'05) confirm the assumption of dizygotic twinning in the common marmoset. The slight deviation of the frequency

Total frequency of abortions, premature births and stillbirths (Category 1) Figure 1 shows the distribution of live-born, aborted, premature or stillborn infants. Twentynine (51'80/0) breeding females had 48 (16'3%) litters which produced 19 (2' 6%) abortions, 7 (0' 9%) premature (including 3 stillborn infants) and 58 (7' 9070)stillborn (including 3 premature) infants. Three females had 3 abortions or stillbirths, and 2 females had 2 abortions or stillbirths. The other 26 females had only one litter which contained non-viable infants. In 7

Table 3. (a) Parity of breeding females and number of litters

Parity n females n litters

to to



6 12






Table 3. (b) Generation Generation n females







3 18

3 21

2 16










1 11




3 39


of breeding females; wb = wildborn;













F = filial generation


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Rothe, Darms & Koenig %


20 19 18 17 16 15 14

13 12 11 10 9 8 7 6 5 4

3 2 1 0 singletons









20 19 18 17 16 15

14 13 12 11 10 9 8 7 6 5 4

3 2 1

0 singletons

Fig. 2. Relative frequency of abortions and stillbirths of singletons, twins, triplets and quadruplets in relation to: (A) the total number infants born; and (B) the total number of abortions and stillbirths: 0, unsexed; _, females; !;:I, males.

(12' 3070) pnmiparous females all infants were stillborn or aborted (4S, lTw, lTr, lQ), 6 (10'5%) primipara gave birth to a mixed set of living and dead infants and for 44 (77 . 2%) primiparous females all infants

were live-born. As a whole, 14 294 sets of :nfants contained infants {the above-mentioned 7 primipara and 7 additional sets 3Tr».

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(4'807o) of only dead sets from (IS, 3Tw,

Sex ratio and mortality

in the common



frequency of stillborn and aborted infants in relation to the total number of infants born in each litter reveals significant differences between parity 1 to 13 (x2=38'74, df= 12, P 16'27; df=3; P 16·27; df = 3; P

Sex ratio and mortality in a laboratory colony of the common marmoset (Callithrix jacchus).

In a retrospective study sex ratio and mortality were analysed in a captive colony of common marmosets (Callithrix jacchus). Seven hundred and thirty-...
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