Apr 27, 2008 - 0·9 x 0·9 x 0·5 m (height), usually with a hardboard inner wall 0·75 x 0·75 x 0·30 m (height) to prevent the shrews from escaping. The enclosures.
359
Laboratory Animals (1984) 18, 359-363
Breeding the common shrew (Sorex araneus) in captivity J. B. SEARLE* Department of Genetics. University of Aberdeen, United Kingdom Summary A method for the systematic breeding of the common shrew (Sorex araneus) is described. By use of this method 20 litters of common shrew, conceived in the wild and in captivity, were reared to weaning. Successful fertilization was recorded for 74% of pairings and 68% of young known to have been born were reared to weaning. Breeding records indicate that common shrews will mate within a few days of pairing and that the duration of pregnancy and lactation is about 43 days. The common shrew is one of the most widespread and abundant species of insectivore found in the northern Palaearctic and is an animal of considerable biological interest. Studies of this species have been hampered by the absence of a reliable method of breeding in captivity. The common shrew is one of the most karyotypically variable small mammals and, as noted by Fredga & Narwin (1977), breeding studies can be used to assess the degree of reproductive isolation of karyotypically different forms. However, only now, using the method described in this paper, have such studies been attempted (Searle, 1984). The method has also been used to examine the inheritance of white-spotting and electrophoretic variants for the first time (Searle, 1983 and in preparation). Attempts to breed the common shrew in captivity have been reported in the literature, and Dehnel (1952), Vogel (1972a), Vlasak (1973) and Fedyk (1980) all managed to rear litters. However, the data of Vogel, Vlasak and Fedyk (Dehne I provides none) indicate that only a small number of litters were reared in each case. In none of these earlier papers is there any indication of success of the programme in terms of proportion of pairings that were fertile or number of young reared to weaning. Nor is it always clear whether litters were conceived in nature or captivity. 'Present address: Department of Agricultural Science, University of Oxford, Parks Road, Oxford OX I 3PF, United Kingdom Received
20 February
/984. Accepted
27 April
/984.
Tillydrone Avenue, Aberdeen AB9 2 TN,
In this paper, the methods and results are given for a programme of breeding wild-caught common shrews carried out in 1980 and 1981. The methods were suited to particular research requirements but can be adapted readily. It is believed that the procedure described in this paper for breeding the common shrew is the first for which there is substantial evidence of a high success rate and repeatability. No attempt was made to breed from the animals reared in captiv.ity and so initiate a continuous breeding colony as has been achieved for whitetoothed shrews (e.g. Crocidura russula: Hellwing, ]971). However, it should be noted that such a continuous breeding colony is a real possibility, given that the following have been achieved: a. a reliable breeding method (this paper); b. a simpler method for long-term maintenance (Gray-Wallis, 1984); c. a method for inducing sexual maturity in immature animals in captivity (Crowcroft, 1964).
Materials and methods Housing 2 types of cage were used: box cages and enclosures. Both types of cage were kept outdoors on the flat roof of the Department of Zoology, University of Aberdeen, the box cages stacked within an open shed. Box cages were wooden and of dimensions 0·30 x 0·45 x 0·25 m (height) with a removable glass front and perforated zinc cover, after a design by Dehnel (1952). They were either used singly or 2 such cages were strapped together and connected by an aperture to form a 'double cage'. The enclosures were made of heavy duty clear polythene and were 0·9 x 0·9 x 0·5 m (height), usually with a hardboard inner wall 0·75 x 0·75 x 0·30 m (height) to prevent the shrews from escaping. The enclosures were protected from rain by a sloping roof of clear polythene and from birds by garden netting which covered the whole enclosure including the gaps left for ventilation. The substratum to both types of cage consisted of earth, peat and turf sods. To maintain the cool, moist conditions preferred by shrews in captivity (Hutterer, 1977), this substratum was regularly sprinkled with water. In each box cage I nest box was
360
Searle
provided; the enclosures had at least 2 nest boxes. These nest boxes were filled with hay, paper towels and paper tissues or cotton wool and in the enclosures they were placed under a substantial covering of loose earth and turf sods to protect them from direct sun. A hamster wheel was usually provided in box cages.
Procedure Adult common shrews were collected in Longworth live traps during late May and June. At this time most, and probably all, females used would have been
primigravid
or parous (Brambell,
] 935) and many
were found to be pregnant on capture (see below). The animals were fed with homogenized ox heart moistened with water and carefully transported from the site of capture to the laboratory in deep buckets with moist peat and hay as nesting materials (Searle, 1983). The animals were sexed (Searle, in preparation), and adult females and males were placed singly in box cages and enclosures, respectively. The mating procedure adopted reflects a dual interest in (a) breeding in captivity from specific pairings and (b) the maintenance through to weaning of pregnancies conceived in nature. If only litters conceived in captivity are required, it would be convenient to isolate wild-caught females for the full gestation period of 20 days (Vogel, 1972b; Dehnel, 1952) and kill any litters produced (which would have been conceived in the wild) before introduction to a male. In the present study, both types of litter were of value and, therefore, it was only necessary to delay pairing for a few days in order to be able to determine, by extrapolation from the date of weaning, whether litters born subsequently were conceived in the wild or in captivity. Thus, each newly captive female was isolated for a period of at least 7 days in a box cage. After the isolation period, the box cage of the female was examined for the presence of young. If young were present, the box cage was expanded to a double cage and the female permitted to rear her litter undisturbed. If no young were present, the female was transferred to an enclosure which housed a male. Each male had been kept in the enclosure for a period (generally 2 days) prior to pairing, to become accustomed to the surroundings; this may be important for libido (S. Fedyk, personal communication). The pair was left for 8 - 21 days to allow mating to occur where the female was not already pregnant. After this period, both adults were quickly removed by hand from the enclosure, which was then thoroughly searched for young. It was considered important that a male should not be left with an unattended litter (Crowcroft, 1957). If young were present, the female was returned to the
enclosure and allowed to rear her litter to weaning in the absence of the male and with minimum disturbance. If no young were present, the male only was returned to the enclosure and a new pairing set up after a few hours. The female was placed in a double cage or another enclosure, in which, if she was pregnant at the time of separation from the male, she could rear her litter in isolation. The cage was checked once or twice to determine if a litter had been produced. Females which had no litters after one attempted pairing were often remated. The young were separated from their mothers at weaning. Dehnel (1952) noted that mother and young are aggressive towards each other after this time. On the basis of the litters maintained beyond weaning in this study, it does appear that the young will live together without fighting for at least a few days after weaning. Weaning is easily determined. Vogel (1972b) has shown that weaning occurs at the same time as tooth eruption and when the young first feed themselves. The sign of the first feeding of young was always very obvious; there was a sudden increase in the amount of food eaten and the food dishes became unusually dirty. A major rationale behind this procedure was to disturb the breeding shrews as little as possible. No attempt was made to monitor females so that they could be mated at times of particular receptivity, e.g. the postpartum oestrus and post-weaning oestrus identified by Dehnel (1952). In this particular study, females were generally killed after rearing 1 litter to weaning; clearly, in other studies they could be used for further pairings.
Feeding The breeding diet was similar to that of S. Fedyk (personal communication) and P. Vogel (personal communication), and contained the following ingredients in the proportions (by weight) as indicated: 34 parts fresh ox heart; 22 parts fresh chicken (removed from bone); 11 parts fresh ox liver; 11 parts cracked wheat; 11 parts rolled oats; 10 parts raw chicken eggs (shells removed); 1 part 'Vionate' vitamin and mineral supplement (E. R. Squibb, Twickenham, Middlesex); 1 part 'Zusatz fUr Fleischfresser' vitamin and mineral supplement (NAFAG, Gossau, Switzerland). The meat and eggs were homogenized with a small quantity of water. The diet was stored at -20°C after thorough mixing of the components. The food was moistened and presented in 5-cm diameter plastic petri dishes (approximately 15 g breeding diet per dish) twice daily at about 08.00 h and 18.00 h. As a general rule, at each time of feeding, the shrews were rationed as follows: 1 dish per adult for mating shrews and during early pregnancy; 2 dishes during late pregnancy and the
Breeding
common
first week or two of lactation; and 3-4 dishes during late lactation and around the time of weaning. However, there was great individual variation in feeding habits and some animals required larger quantities of food than the standard.
and discussion Evaluation of breeding programme
Results
2 indices were used to assess the success of the breeding programme: firstly, the fertility of attempted pairings and secondly, the survival of the young to weaning. In the following analysis, results from both years when shrews were bred in captivity (1980 and 1981) are considered together to provide an adequate data base. Similar numbers of young and litters were reared in each of the 2 years. Successful fertilization was usually identified by whether young were born and was recorded in 17 (74%) of 23 attempted pairings. This is probably an underestimate, since if the young were lost before or soon after birth they would most likely have gone undetected. The number of young and of litters known to have been born in captivity are shown in Table 1. Altogether 101 (68%) of 149 young were successfully weaned in captivity. Both behaviourally and anatomically these weanlings were similar to recently weaned shrews caught in the wild, though they tended to be heavier, probably as a consequence of fat deposition. For example, in 1980 the weight (mean ± S E) of captive-bred animals, determined within 16 days of weaning, and of immature shrews from Dinnet (Grampian, Scotland) caught early in the breeding season in June, 1980 was 8·38 ± 0·13 g (n = 47) and 6-47 ± 0·20 g (n 11) respectively; (t = 6·63, d.f. = 56, P
=
< 0'001). There was no evidence that the conditions
of captive breeding had an unequal effect on the survival of the 2 sexes. Overall, 54 (55%) of 98 weaned shrews that were sexed were male; this sex ratio did not differ significantly from equality (X2 =
1,02, d.f. '= 1, P
361
shrews
> 0·05).
20 (69%) of the 29 litters recorded were reared to weaning, although in 2 of these litters there was evidence of pre-weaning loss. Of the 7 litters completely lost through 'natural causes', 5 (all of which were conceived in the wild) could be accounted for by death of the mother or inadvertent long-term seperation of mother and young. It is clear from Table 1 that there was greater loss of young conceived in the wild than in captivity. This may be a consequence of the better care afforded to the maintenance of females paired in captivity (see above). However, of those litters that were reared to weaning similar numbers of young per litter (mean ± S E) survived to weaning for litters conceived in captivity and in nature (4·8 ± 0·5 (n =
12) and 5·4 ± 0·7 (n = 8), respectively; t = 0·63, d.£. = 18, P > 0·05). In conclusion, by the indices of fertility following pairings and the survival of young to weaning, the breeding programme adopted in this study was highly successful. With experience, it is considered that the breeding performance could be improved still further.
Reassessment of reproductive parameters As a by-product of a breeding programme, information on a variety of reproductive parameters becomes available and this may be used to improve the planning of future breeding programmes. In this section data on the length of the pre-weaning development period and the duration of the period between pairing and successful copulation are considered.
The length of the pre-weaning development period As the shrews were only examined intermittently during the breeding programme, the time when a female mated or gave birth was never determined accurately. However, a useful estimate of the maximum or minimum length of the pre-weaning development period could be calculated for some litters from the following information: a. the date of weaning b. the date when a pairing was set up or when a shrew was captured and c. results of routine examinations of the cage to determine presence or absence of a litter. For individual litters, the greatest minimum estimate of the length of the pre-weaning development period was 44 days and the smallest maximum estimate was 43 days (Table 2). Thus it seems reasonable to conclude that, under the
conditions
adopted
in this study, the period of
gestation and lactation totalled 43-44 days in the common shrew. This result concurs with the findings of Dehnel (1952), who quoted a gestation period of 20 days and a lactation period of 23 days in his study on reproduction of the common shrew in captivity. The results of Crowcroft (1957) suggest a similar length of gestation and lactation, while Vogel (l972b) gave a lactation period of 26 days. The lower estimates of Brambell (1935) of the period of pregnancy and lactation are liable to be incorrect, as they are extrapolations from material collected in the wild. If, as proposed by Dehnel, Crowcroft and Vogel, the lactation period is longer than the gestation period, embryos conceived at the postpartum oestrus will have to remain ill lIIero for longer than the standard gestation period (Vogel, 1972a). The length of time to mating Taking the length of the period of pre-weaning development' to be 43 days (see above), an estimate of the time between
Searle
362 Table 1. Details of number of young (A) and number of litters (B) reared in captivity (A)
Tota/llO. known to have been born Conceived the wild
in
80
Conceived captivity
in
Total
No. killed before weaning
29
43
69
7
4
58
149
15
33
101
Tota/no. known to have been born in
15
Conceived captivity
in
14
No. killed hefore weaning I
No. complete /il/ers /OSI before weaning
No. wealledt
6
8 (8)
12 (10) 2
29
Total
20 (18)
7
·Number known to have been lost through 'natural causes' tThe number of litters in which all young were successfully parentheses
weaned
are shown
Table 2. Frequency of maximum and minimum estimates of the duration of the pre-weaning developmental period * Duration (days)
No. of casest Min. estimate Max. estimate
30-41
42
2 2
44
2
43
No. weaned
8
(B)
Conceived the wild
No. died before weaning"
I
2
45
2 2
46-55
6
• All minimum estimates of less than 30 days and all maximum estimates of greater than 55 days are excluded t Each case represents the sole estimate from a single pairing
In known
Breeding
common shrews
introduction of female to male and successful copulation could be made for all those pairings where the time of weaning was determined accurately. Of 5 such matings where it could be certain that the female was not pregnant or lactating on introduction to the male, all successful copulations occurred within 4 days of introduction (i.e. within half the minimum time of 8 days made available for mating), with a mean time of 2·0 days. These results suggest that the period made available for mating in this breeding programme (8-21 days) was longer than necessary for a pairing involving a female that is not pregnant or lactating.
363
Acknowledgements I am very grateful for the advice given to me by Dr S. Fedyk (Mammal Research Institute, Bialowieza, Poland) and Professor P. Vogel (University of Lausanne, Switzerland). I also thank Dr J. R. Clarke, Dr A. E. Douglas and P. J. Wilkinson (University of Oxford) for comments on an earlier draft of this paper. This work formed part of a PhD project supervised by Professor F. W. Robertson and funded by S.E.R.C.
References Brambell, F. W. R. (1935). Reproduction in the common shrew (Sorex araneus Linnaeus). I. the oestrous cycle of the female. Philosophical Transactions oj the Royal Society oj London B 225, 1-49. Crowcroft, P. (1957). The LiJe oj the Shrew. London: Reinhardt. Crowcroft, P. (1964). Note on the sexual maturation of shrews (Sorex araneus, Linnaeus 1758) in captivity. Acta Theriologica 8, 89-93. Dehnel, A. (1952). The biology of breeding of the common shrew (Sorex araneus L.) in laboratory conditions. Annales Universitatis Mariae Curie Sklodowska C 6, 359-376. Fedyk, S. (1980). Chromosome polymorphism in a population of Sorex araneus L. in Bialowieza. Folia Biologica Krakow 28, 83--120. Fredga, K. & Narwin, J. (1977). Karyotype variability in Sorex araneus L. (Insectivora, Mammalia). Chromosomes Today 6, 153--161. Gray-Wallis, J. (1984). Maintenance of the common shrew, Sorex araneus, under laboratory conditions. Animal Technology (in press). Hellwing, S. (1971). Maintenance and reproduction in the white toothed shrew, Crocidura russula monarcha Thomas, in captivity. Zeitschrift fiir Siiugetierkunde 36,
Hutterer, R. (1977). Haltung und Lebensdauer von Spitzmausen der Gattung Sorex (Mammalia, Insectivora). Zeitschrift fiir Angewandte Zoologie 64, 353--367.
Searle, J. B. (1983). Robertsonian chromosomal variation in the common shrew Sorex araneus L. PhD Thesis, University of Aberdeen, Scotland. Searle, J. B. (1984). Hybridization between Robertsonian karyotypic races of the common shrew Sorex araneus. Experientia (in press). Vlasak, P. (1973). Vergleich der postnatalen Entwicklung der Arten Sorex arafleus L. und Crocidura suaveolells (Pal!.) mit Bermerkungen zur Methodik der Laborzucht (Insectivora: Soricidae). Vestnik Ceskoslovellske Spolecnosti Zoologicke 37, 222-233. Vogel, P. (1972a). Beitrag zur Forlplanzungsbiologie dcr Gauungen Sorex, Neomys und Crocidura (Soricidae). Verhandlullgen der Naturforschelldell Gesellschaft ill Basel 82, 165-192. Vogel, P. (1972b). Vergleichende Untersuchung zum Ontogenesemodus einheimischer Soriciden (Crocidura russula, Sorex aralleus und Neomys fodiens).Revue Suisse de Zoologie 79, 1201-1332.
103--113.
Zucht der Waldspitzmaus (Sorex araneus) in Gefangenschaft J. B. SEARLE Zusammenfassung: Es wird eine Methode zur systematischen Zuchl der Waldspitzmaus (Sorex araneus) beschrieben. Mit Hilfe dieser Methode wurden 20 Wiirfe von Spitzmausen, die in der Natur und in Gefangenschaft gedeckt worden waren. bis zum Absetzen grol3gezogen. Erfolgrciche Befruchtung
wurde beobachtet bei 74% der Verpaarungen, 6WVu der Jungen, die als geboren registricrt waren, daB sich die Spitzmiiuse innerhalb weniger Tage nach dem Zusammensetzen verpaaren und daB die Dauer der Triichtigkeit und Laktation etwa 43 Tage betriigt. (G)
