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Maintenance and reproduction of tenrecs (Tenrecidae) at Parc Tsimbazaza, Madagascar

Peter J. Stephenson1, Paul A. Racey1 & Félix Rakotondraparany2
1Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen AB9 2TN, Great Britain and 2Département de Zoologie, Parc Botanique et Zoologique de Tsimbazaza, BP 4096, Antananarivo 101, Madagascar


From: International Zoo Yearbook 33 (1994): pp 194-201. Published by the Zoological Society of London.
Online publishing with kind permission of the International Zoo Yearbook and the Zoological Society of London.
© The Zoological Society of London. Online conversion by David Kupitz.

An extensive captive-breeding programme for tenrecs was carried out over a two-year period in Madagascar. Six of the 12 species studied gave birth in captivity and valuable data on diet, reproduction and growth rates were collected.

The Tenrecidae (Mammalia, Insectivora) includes an ancient lineage of eutherian mammals endemic to Madagascar (Eisenberg & Gould, 1970). The family is comprised of three subfamilies, the Tenrecinae and Oryzorictinae of Madagascar, with eight genera and 26 species, and the Potamogalinae, the otter-shrews, from Africa (Genest & Petter, 1974; Corbet & Hill, 1991; Stephenson, 1991, in press). The reproductive biology of the Tenrecinae is relatively well studied (Gould & Eisenberg, 1966; Eisenberg & Gould, 1967; Riordan, 1972; Godfrey & Oliver, 1978; Nicoll & Racey, 1985) but the only data available on reproduction in the Oryzorictinae arise from two species of Microgale kept in captivity in the USA (Eisenberg & Gould, 1970; Eisenberg & Maliniak, 1974; Eisenberg, 1975). As deforestation threatens tenrec habitats in Madagascar (Nicoll & Rathbun, 1990; Stephenson, 1993a), there is an increased need to establish captive populations and understand breeding techniques. Currently no species of Oryzorictinae are held in captivity outside Madagascar.

This paper documents the most extensive tenrec captive-breeding programme ever undertaken in Madagascar. Between April 1988 and June 1990, four species of Tenrecinae and eight species of Oryzorictinae were maintained at the Parc Botanique et Zoologique de Tsimbazaza, Antananarivo (Table 1). Six species gave birth in captivity. We outline captive-maintenance techniques at Tsimbazaza and provide new data on reproduction and neonate growth rates.

Species No. individuals Origin
Males Females
Tenrecinae
Setifer setosus 2 2 Analamazaotra (18°28'S, 48°28'E)
Hemicentetes nigriceps 2 2 Ambohimahasoa (21°06'S, 47°12'E)
H. semispinosus 3 6 Analamazaotra
Echinops telfairi 4 4 Beza Mahafaly (23°40'S, 44°32'E)
Oryzorictinae
Oryzorictes hova 0 1 Analamazaotra
Microgale cowani 3 4 Ambohitantely (18°09'S, 47°16'E)
M. dobsoni 4 11 Ambohitantely
M. longirostris 1 1 Anjozorobe (18°23'S, 47°53'E)
M. melanorrhachis 1 1 Analamazaotra
M. talazaci 4 12 Analamazaotra
Limnogale mergulus 1 0 Ranomafana (21°15'S, 47°26'E)
Geogale aurita 9 13 Beza Mahafaly

Table 1. Tenrec species brought into captivity at Parc Botanique et Zoologique de Tsimbazaza between April 1988 and June 1990. The nomenclature for shrew-tenrec species follows Stephenson (in press).

Maintenance

Enclosures   Two types of enclosures were used. (1) Wooden box cages measuring 100 x 50 x 55 cm deep were used to house tenrecine species. Each box contained a nestbox 30 x 23 x 22 cm high which had a removable lid to facilitate cleaning. The lid and walls of the enclosure had wiremesh sections to assist air circulation and allow light into the box. Smaller box cages measuring 58 x 55 x 55 cm deep with a nestbox measuring 23 x 20 x 12 cm high were built to house Microgale talazaci. (2) Glass aquaria measuring 56 x 26 x 26 cm deep were fitted with a wooden lid, punctured with numerous air holes. Aquaria were used to house Geogale aurita, Oryzorictes hova, Microgale dobsoni, M. cowani, M. melanorrhachis and M. longirostris.

Wood shavings were used as substrate, at least 1 cm deep, and dry grass was provided as nest material. In the wooden boxes the grass was placed in the nestbox. In the aquaria grass was usually placed in one corner except for the aquarium housing O. hova where grass was placed over the whole floor to a depth of several centimetres. Aquaria containing G. aurita were provided with an abundance of bark and 1.8 cm diameter cardboard tubes. Females in late pregnancy or lactation preferred to remain under bark.

Cages were checked daily. Faeces and food debris were removed and wood shavings replaced where necessary. Nest material was replaced weekly or when fouled.

A solitary male aquatic tenrec Limnogale mergulus was held at Tsimbazaza between June and July 1989. This animal was caught at Ranomafana by Edwin Gould of the Smithsonian Institution who constructed a wooden box enclosure with access to a large aquarium through a system of plastic tubing. Leaves were provided as bedding inside the box. The aquarium was filled with water to a depth of > 20 cm and a rock was provided as a feeding platform. After six weeks the animal was released at its capture site.

Feeding regimes   The tenrecs were fed on natural prey items, freshly caught each morning in the Park grounds, whenever possible (Table 2). The diet was supplemented with locally purchased fruit and beef mince. Occasionally, G. aurita was offered termites collected from Réserve Spéciale d'Analamazaotra.

Tenrecs were fed once daily between 1600 and 1800 hours. The weight of food given to each species varied according to body size and appetite. In the winter, most tenrecines were torpid so less food was required. All tenrec species that bred required increased food during pregnancy and lactation when metabolic rate was elevated (Stephenson & Racey, 1993a, b, 1994).

Shrew-tenrecs Microgale spp generally have higher metabolic rates than other tenrecs (Stephenson & Racey, 1993b) and have correspondingly voracious appetites. Microgale spp were always offered an abundance of food so that some remained in the enclosure the following morning. Limnogale mergulus is known to feed on frogs, crayfish, crab and aquatic insects (Malzy, 1965). At Tsimbazaza the male was offered crab and fish but only fed readily on frogs. During six weeks in captivity this animal maintained body weight of 75-80 g but, in the future, the long-term survival of captive individuals may depend on their eating other natural prey items.

Species Food items
Orthopteran
insects
Earthworms Frogs Beef
mince
Fruit Fish Crabs Termites
Setifer setosus 1 1 2 2 2      
Hemicentetes nigriceps   1            
H. semispinosus   1            
Echinops telfairi 11 1 2 2        
Oryzorictes hova   1            
Microgale cowani 11 2 2          
M. melanorrhachis 11 2 2          
M. longirostris 11 2 2          
M. dobsoni 1 2 11          
M. talazaci 1 2 11          
Limnogale mergulus     11     1 1  
Geogale aurita 1             2

1Preferred food item if a preference was apparent.
Table 2. Diets for tenrecs in captivity at Parc Tsimbazaza. 1 = daily food item, 2 = occasional food item. Fruit was banana or mango and was offered only in the summer.

Torpor   Seasonal hypothermia occurred in Setifer setosus, Echinops telfairi, Hemicentetes semispinosus and H. nigriceps between June and September. During the winter months, G. aurita underwent daily torpor. The level of activity and the reduction in metabolic rate varies between species (Stephenson & Racey, 1994). Throughout the winter G. aurita and H. semispinosus fed regularly although the other hibernating species did not require regular feeding during this time.

Longevity   Small species of Microgale were difficult to maintain for prolonged periods. Microgale cowani, M. melanorrhachis and M. longirostris fed well and maintained or gained weight but never survived more than ten weeks. Larger oryzorictines were easier to maintain. One female M. dobsoni died after 18 months in captivity; based on its body size at time of capture this animal must have been at least two-and-a-half years of age. A female M. talazaci, which produced two litters in her second year in captivity, must have been at least two-and-a-half years old.

Once established in the colony, all tenrecines lived for more than a year. At least one male H. nigriceps lived for more than three years. The longest surviving H. semispinosus and S. setosus lived more than 15 months at Tsimbazaza.

The most common cause of death among adult tenrecs was roundworm infection. Individual G. aurita, M. talazaci, H. semispinosus and H. nigriceps contracted parasitic worm infections of the peritoneal cavity. In most species we could not determine whether or not the worm infection was the primary cause of death but in G. aurita the worms were so large that they filled the body cavity and must have proved fatal. Worming tablets or powders are not readily available in Antananarivo but they will be essential if future captive colonies are to survive.

Captive-breeding techniques

Outside the breeding season animals were often kept in mixed-sex groups. At the onset of the breeding season around September/October all species showed aggressive behaviour towards members of the same sex and the animals were then isolated or paired. Whenever possible the male and female were introduced into a freshly cleaned cage simultaneously to prevent possible territorial conflict.

Prior to parturition males were usually separated from females, though occasionally they were left in the enclosure for 48 hours to allow for the possibility of post-partum matings.

The tenrecs were observed frequently to ascertain dates of reproductive activity. Nests of pregnant females were checked regularly to determine parturition date. Neonates were weighed within seven days of parturition and their body measurements were recorded on average once per week to determine growth rates. Infants were handled as little as possible throughout and, during the first month, always through a cloth bag that had previously been used to hold the mother.

Reproduction

Six species gave birth to 23 litters (Table 3) of which 19 were conceived in captivity. The M. cowani litter, one litter of M. talazaci and two litters of M. dobsoni were produced by females taken into captivity while pregnant.

Attempts to breed S. setosus were unsuccessful. Two pairs were maintained and one pair was together for two breeding seasons but neither showed any signs of reproductive activity. The pair of M. longirostris were only held for two weeks. The other species held in captivity were either held as singletons (O. hova and M. melanorrhachis) or they were not paired (E. telfairi).

Geogale aurita was the most prolific breeder with ten individual females producing 13 litters over the two years. Four females conceived on the day of parturition and were pregnant with a second litter while suckling the first. This is the only species of tenrec known to exhibit post-partum oestrus (Stephenson, 1993b).

Two M. dobsoni bred both years producing a single litter each. One M. talazaci bred both years producing one litter the first year and two litters in the second. In M. cowani, H. semispinosus and H. nigriceps single litters were produced in the first year and none in the second (Table 3).

Species Year 1 Year 2
No. females
breeding
No. litters No. females
breeding
No. litters
Hemicentetes nigriceps 1 1    
H. semispinosus 1 1    
Microgale cowani 1 1    
M. dobsoni 2 2 2 2
M. talazaci 1 1 1 2
Geogale aurita 5 7 5 6

Table 3. Captive tenrec births at Parc Tsimbazaza between September 1988 and March 1989 (Year 1) and between September 1989 and March 1990 (Year 2).

Parturition   Parturition dates varied significantly between each year. In the first year births occurred between 11 November and 31 January. In the second year births were generally much later with seven of the ten litters being born after 31 January. However, overall timing of parturition was more varied with births occurring from 4 September to 29 March.

The factors affecting the onset of breeding in the Tenrecidae are poorly understood. Endogenous rhythms controlling annual activity cycles may be synchronized by ambient temperature or photoperiod (Stephenson & Racey, 1994) and the same factors might influence reproduction. Certainly, gestation length in at least some tenrec species is variable and may be influenced by ambient temperatures (Stephenson & Racey, 1993a).

Litter survival   Offspring survival was variable. The first litter of M. talazaci, and the M. cowani and H. semispinosus litters were attacked or eaten by the mother within two days of parturition. In each instance the minimal disturbance necessary for routine maintenance appeared to be a contributory factor: the female M. cowani consumed her litter of three after they had been removed from the nest for no longer than ten seconds each to be weighed. Other species were less affected by disturbance. Microgale dobsoni were generally more passive than M. talazaci and individuals rapidly became habituated to handling and females showed no adverse behaviour towards the litter, even if the offspring were touched within the first few days after parturition. Similarly, G. aurita neonates could be handled within the first few days of birth with no adverse reaction from the mother.

All M. dobsoni litters, two M. talazaci litters and the litter of H. nigriceps weaned and grew to adulthood. For unknown reasons only one G. aurita infant survived while the others lost weight rapidly after weaning and died. Fresh or powdered milk has been used successfully in the rearing of other tenrec species outside Madagascar (Louwman, 1973; Eisenberg & Maliniak, 1974) so we supplemented the diet of older G. aurita infants with powdered milk but this did not improve their survival rate.

Growth and development   All tenrecs are highly altricial and are born naked with both the auditory meatus and eyes closed. Development rates, as measured by growth rates and times to eye-opening and weaning, varied between species (Table 4).

Age at weaning was often difficult to distinguish because infants showed an interest in solid foods before becoming completely independent of the mother. In addition, many attempted to suckle long after weaning was initiated; for example, M. dobsoni young were recorded trying to suckle at day 56, even though they had been consuming solids since day 27. As a rule infants started actively seeking food soon after eye-opening. Microgale dobsoni and M. talazaci readily attacked and consumed prey at eye-opening withing four weeks of parturition. Eye-opening in Hemicentetes spp occurred withing two weeks but they were not seen feeding on solid foods until they were three weeks old. The slowest to wean were G. aurita which did not become independent until five weeks of age. However, their body mass reached a peak at weaning and then began to decrease, possibly due to an inadequate diet. The young may have weaned sooner if smaller prey, such as termites, had been available more frequently.

Species Maternal body
mass (g)
Litter size Neonate
mass (g)
Growth rate
(g/day)
Age at eye-
opening (days)
Hemicentetes nigriceps 113 3 8.3 0.71 7-12
H. semispinosus 133.5 7 8.3   7-10
Microgale cowani 10.3 3 2.5    
M. dobsoni 44.2 1-5 (3-8) 3.7 0.23 25-27 (26)
M. talazaci 46.6 (3) 3.7 0.25 28
Geogale aurita 6.9 2-5 (3.9) 0.7 0.06 21-33 (24.3)

Table 4. Data on reproduction in tenrec species breeding at Parc Tsimbazaza. All values represent means except for litter size and age at eye-opening where ranges are represented with mean values in parentheses.

Influence of litter size on development rate   From data on litter mass immediately after parturition, there is evidence that neonates from larger litters are smaller at birth than those from smaller litters. In M. dobsoni, mean neonate mass within two days of birth was 4.9 g in a litter of four but 3.3 g in a litter of five, and in G. aurita mean neonate mass in a litter of three was 0.83 g and in a litter of five was 0.63 g.

Growth rates of G. aurita, M. talazaci and M. dobsoni neonates were generally faster in smaller litters (Table 5). Therefore, although accurate data are scarce, there seems to be a trend for neonates from smaller litters to be larger at birth and to grow more quickly. This follows earlier findings that postnatal growth rate in neonate mammals is dependent on birth weight (Case, 1978). However, eye-opening and possibly weaning are not obviously correlated with litter size.

Litter size Growth rate
Geogale aurita Microgale talazaci Microgale dobsoni
(g/day) (mm/day) (g/day) (mm/day) (g/day) (mm/day)
1         0.245 1.6
2 0.082 1 0.375 2.3    
3 0.065 0.8 0.115 1.2    
4         0.199 2
5 0.048 0.7     0.23 1.7

Table 5. Growth rates of tenrec neonates from different litter sizes. Growth rates measured as mean increase in body mass per day and mean increase in head and body length per day. Adequate growth data were not available for every litter size produced by each species.

Conclusions

We still have much to learn about captive maintenance and breeding in the Tenrecidae. Small species of Microgale are not easy to maintain for prolonged periods and attempts must be made to improve their chances of survival by experimenting with different and more varied prey. Many species feed on the small invertebrates encountered on the forest floor (Stephenson, 1991, 1993a), so perhaps humus and leaf-litter needs to be provided in the enclosure to stimulate natural foraging behaviour. Mealworms have been used to supplement tenrec diets (Eisenberg & Gould, 1967; Eisenberg & Maliniak, 1974) and may also prove useful with small shrew-tenrecs. Successful breeding of G. aurita may depend on the supply of prey such as termites that are small enough for weaning young to consume.

Many small forest-dwelling tenrecs in the Oryzorictinae may be under threat from human disturbance and habitat loss (Nicoll & Rathbun, 1990; Stephenson, 1993a). Most of these species have not yet been maintained in captivity for more than ten weeks so captive breeding will be a challenge. The aquatic tenrec L. mergulus is probably the most threatened tenrec species (Nicoll & Rathbun, 1990) and this must be the greatest priority for captive-propagation programmes. We have demonstrated that it can be maintained in captivity for six weeks but previously aquatic insectivores have proven difficult to maintain for prolonged periods (Nicoll, 1985). Research into L. mergulus and other oryzorictine tenrecs could be initiated at Parc Tsimbazaza but assistance will be required from zoos outside Madagascar with a firm commitment to conservation.

Acknowledgements

We thank Dr V. Randrianasolo and the keepers at Parc Tsimbazaza for their valuable help and assistance. The Département des Eaux et Forêts (MPAEF) kindly allowed us to work in protected areas. Further support came from the Ministère de l'Enseignement Supérieur and WWF-Aires Protégées. N. Rakotoarison, H. Randriamahaza and E. Rasoimalala provided field assistance. The work was funded by a Natural Environment Research Council studentship to PJS.

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Manuscript submitted 19 May 1993

 

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