The Tenrecs: A Study in Mammalian Behavior and Evolution by J. F. Eisenberg & Edwin Gould, pp. 78-89.
published in Smithsonian Contributions to Zoology No. 27 (1970)
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The Ecology of Hemicentetes (Mivart, 1871)
The genus Hemicentetes contains two species, H. semispinosus and H. nigriceps. These animals show a high tooth number, with a dental formula of 3/3 1/1 3/3 3/3 for a total of 40 teeth. The teeth, however, show a reduction in size and, when compared with that of the other genera, the skull is markedly elongate and delicate. Hemicentetes possesses quills scattered on its dorsum especially concentrated on the crown and in the light colored stripes extending the length of the body. The quills are barbed and detachable with the exception of the modified group of quills in the central posterior region of the dorsum. This group of specialized quills, termed the stridulating organ, is described in the publications by Petter and Petter-Rousseaux (1963), Gould (1965), and Gould and Eisenberg (1966). These quills are enlarged and do not possess barbs and are less easily detached than the other quills on the body (see p. 102).
The animal has a boldly marked color pattern consisting of three main longitudinal stripes contrasting strongly with the black dorsal color. In the case of Hemicentetes semispinosus, the stripes and crown as well as a median stripe on the forehead are yellow. In the case of Hemicentetes nigriceps, there is no median central stripe on the forehead while the crown and body stripes are white. The venter of both species is almost free from spines. The claws on the forefeet are rather stout and some modification for burrowing is indicated (see Figures 2, 48 and 49). As was noted with the other genera, in addition to spines there is a soft underfur far more prominent in H. nigriceps than in H. semispinosus. In addition to fur interspersed with spines, long sensory hairs are distributed over the dorsum. The standard sensory hairs of the facial region are prominent including the mystacial, genal, super-orbital, and mental vibrissae.
The two species are allopatric and indicate slightly different environmental adaptations. H. nigriceps occurs from the vicinity of Manandroy south to Fianarantsoa. It appears to be confined to the central plateau edge. As one descends from the plateau into the true rainforest of the eastern escarpment, one finds Hemicentetes semispinosus. This form has been recorded from Ivohibe to Maroantsetra. We can conclude that H. semispinosus is confined to the rainforest areas below the high plateau extending its distribution to the northern rainforests and south to an undetermined locality below Ivohibe. For convenience we propose to discuss the characteristics and ecology of these species under separate headings.
H. NIGRICEPS - GENERAL ECOLOGY
This plateau-dwelling species is quite similar to the rainforest species with the exception of the difference in color and the fact that the pelage tends to be less spinescent. The underfur is dense and soft and the quills protrude from it so that, overall, the animal has a more woolly appearance. The quills comprising the stridulating organ are less in number on the average than is the case for H. semispinosus (Figure 50). The number of stridulating quills from a sample of 73 H. nigriceps ranges from a low of seven to a maximum of 17; the modal value was 11 quills. There is a difference when age classes are compared since younger animals tend to have more quills than older ones. Although the stridulating quills are replaced if lost, nevertheless, there seems to be a correlation between increasing age and a smaller number of quills (Figure 51).
There are no conspicuous differences between the sexes and the age classes may be defined on the basis of total length. The infant age class ranges from 58.5 to 60 mm for a minimum and 100 to 110 mm in total length at approximately 4 weeks of age. Females may breed at approximately 30 days of age when their total length lies somewhere between 120 and 130 mm. Maximum total length for adult specimens in the field was 180 mm. Field weights for adults range from 80 to 150 grams.
Hemicentetes nigriceps was taken in the plateau area between Manandroy and Fianarantsoa. Its habitat may be characterized as the plateau edge in the vicinity of the transition between eastern rainforest and plateau savannah. Burrows with animals may be found in the vicinity of brush and are generally never far from free water. The cultivation of rice has apparently opened suitable habitats for these animals and they are often found in the vicinity of paddy fields. When the animals utilize cultivated areas for foraging, they may adopt rather atypical habitatas for burrow sites; indeed, in one area (i.e., Manandroy) almost all burrow sites were placed within an introduced eucalyptus forest but their foraging took place in the vicinity of the paddy fields and areas of cultivated manioc (see Figure 52).
From an examination of over 60 burrows, the following generalization can be made. Let us consider a typical case at Manandroy in the eucalyptus forest: Although located in a secondary growth habitat of eucalyptus, tree ferns and other primary elements are still to be found on the fringes of this introduced forest. The ground was covered with rotten logs, branches, and leaves, forming a mat of damp decaying vegetation. The following characteristics of the burrow were noted. It was located in the vicinity of a cultivated field under a rotten log. There was only one entrance to the burrow. The burrow was shallow, approximately 75 mm at the deepest point and around 450 mm long. The burrow entrance was plugged with leaves. Fresh feces were also noted there (Figure 53).
Coleopteran larvae, potential food items, were found in the rotten logs under which the animals tunneled. In addition, worms were found outside the eucalyptus mat in the red-brown soil bear the paddy fields. The burrow provided a rather stable microhabitat for the tenrec. At Manandroy, burrow temperatures were measured for 21 locations. The ambient range was from 20.4° to 30.5° C. Burrow temperatures themselves ranged from 20.5° to 26.5° C. at a distance of approximately 150 to 200 mm from the burrow entrance.
During the course of our field studies, observations were made from 0800 hours through 2300 hours in areas where Hemicentetes nigriceps occurred. Thirteen sightings were made between the hours of 1830 and 2300 hours. One additional animal was trapped sometime between the hours of 0200 and 0600. The field evidence would indicate that in this particular area H. nigriceps is almost entirely nocturnal with the peak activity in the early part of the evening. These observations were amply confirmed in captivity; however, under captive conditions the animals could be conditioned to feed during the daylight hours.
Studies of diel variations in thermoregulation were made in Madagascar both in captivity and in the field. Between the hours of 0900 and 1000, a captive group of five H. nigriceps showed a range of cloacal temperatures from 25.0° to 27.4° C. with an average of 26.3° C. over an ambient range from 23° to 24.2° C. A second series of morning readings was made over an ambient range from 16.8° to 20° C. H. nigriceps showed a cloacal temperature range from 20.8° to 26.4° C. All of these measurements were made during the month of February when the animals are not torpid for long periods. A series of late afternoon temperature readings were made between 1500 and 1800 hours, when the cloacal temperature should be showing an increase. Over an ambient range from 21.3° to 24.3° C., a sample of 14 H. nigriceps showed a range from 26.0° to 31.5° C. with an average of 28.6° C. To compare with this series, several field measurements of body temperatures were made during the early part of April preceding the entry of the population into their seasonal torpid period. Over an ambient range from 22° to 26.8° C., a total of 12 individuals showed a range from 25° to 35° C. with an average of 30.3° C.
Our data would indicate that the animal shows a diel fluctuation in body temperature with the cloacal temperature rising in the late afternoon preceding activity. The burrow undoubtedly serves to aid in conservation of heat loss and to ameliorate the more drastic changes in the ambient temperature.
The Annual Cycle and Reproduction
Annual variations in weight and activity were studied in the field and in the laboratory. From a period of 31 January to 3 February 1966, weights were determined for adult animals in the field. Eleven adults ranged in weight from 90 to 150 grams. Four H. nigriceps were returned to the laboratories at the National Zoological Park for further study. During the month of April our captive group of four attained weights from 135 to 187 grams. From the middle of April until July, this group ceased to feed, declined in weight, and did not significantly thermoregulate with the cloacal temperature remaining near the ambient. Minimum weights of 90 to 145 grams were achieved at the end of this period. Beginning in late July and early August, the animals increased their activity, began to feed, and new maximum weights were achieved in December of 1966, exceeding the previous maximum.
With no special manipulation of food or ambient conditions in the laboratories, the captive group began to show weight declines as early as December 1966 for one individual and as late as March 1967 for two others. These declines persisted until July of 1967 when the animals began to arouse, thermoregulate, and feed again. These captive data support previously recorded field observations. In the vicinity of Manandroy and Fianarantsoa, the population of H. nigriceps is generally torpid during June and July.
It would appear that the seasonal torpidity shown by H. nigriceps is in part under endogenous control, since the rhythm persisted through two seasons in captivity with no special attempt to manipulate environmental conditions. Thus, two types of thermoregulation are exhibited. During the breeding season extending from September on into February, the animals show a diel rhythm in thermoregulation but arouse during each 24-hour period to feed. In early May the animals, having reached their full weight, enter a profound torpor which parallels the austral winter.
Population of Hemicentetes nigriceps were sampled in February of 1966 and 1967. The gestation for nigriceps is similar to that displayed by H. semispinosus which is about 58 days. H. nigriceps gestation exceeds 55 days and is less than 58 days; thus it seems reasonable to assume that it is approximately the same for the two species. The litter size for H. nigriceps in wild-caught individuals excavated from their burrows during the month of February 1966 ranged from one to three with an average of 1.4 for a sample of 14 litters. During the same season in 1967, the litter size ranged from one to five with an average of three for a total of six litters. Litter size determined from captive born animals for a sample of five ranged from two to four with an average of 2.8.
The age classes for Hemicentetes nigriceps have been determined from extensive captive studies. For the purposes of our discussion, we have referred to animals in the 60 to 90 mm total length size class as infants. Juveniles include the group from 100 to 130 mm total length and adults are all those animals exceeding 130 mm total length. Although the breeding for our population of H. nigriceps was not completely synchronized, the evidence strongly suggests that breeding begins in early September and most of the first born females in the population probably become pregnant from the period of December to early January. We infer this from a knowledge of the growth curve and of the gestation period.
For example, from 28 January to 7 February 1966, collections of individuals from Manandroy were marked and released. Of the 56 individuals measured, 10 fell in the infant class, 15 were juveniles, and 31 were adults. A similar sample of 33 taken at Manandroy from 6 to 7 April 1966 indicated 8 individuals in the juvenile age class and the remaining 25 as adults. In the following year from 4 to 5 February 1967, the Manandroy population was again sampled and a total of 48 individuals were measured. Of these, 9 were infants, 9 were juveniles, and the remaining 30 adults. This would appear to substantiate our contention that some breeding takes place in December; however, a consideration of the animals in the 130 to 150 mm age class (on the basis of pelage color and wear) suggests that some births may take place in early November. Thus, there must be a first breeding period in early September or the individuals in this size range have wintered over from the previous year having been born late in April of the preceding season. The latter hypothesis is doubtful in view of our knowledge of the growth curve. As indicated previously the Manandroy population was always marked and released. Collections for captive studies were made at Alakamisy Ambohimaha. We know from our captive records that animals may live to an age exceeding 2 years and 6 months. We know further from our sampling in 1966 and 1967 that marked individuals may survive to a minimum age of 15 months. Since females become sexually mature within 4 to 5 weeks of their birth, it is entirely possible that a given female will reproduce in two consecutive breeding seasons.
In captivity, Hemicentetes nigriceps readily accepted earthworms. To a lesser extent, H. nigriceps would kill and eat the larger coleopteran larvae found in the rotten logs under which it nested. Orthopterans were not taken. H. nigriceps could be induced to take some raw chopped meat in captivity, but the animals could be maintained in good condition only if considerable numbers of worms were fed. Two H. nigriceps were collected at night while feeding. Their stomach contents consisted almost exclusively of earthworms although an arachnid abdomen was identified. Soem earth, evidently ingested with the worms, was present in both stomachs. Since earthworms appear to account for a large portion of the animals' diet, it seems desirable to review some of the characteristics of earthworm ecology and behavior.
EARTHWORM BEHAVIOR AND ECOLOGY
Lumbricus terrestris shows a minimum of activity between 0700 and 1100 hours. High rates of activity are shown before 0700 and after 1100 hours. Peak activity is shown in the early mid-afternoon lasting through early morning (Laverach, 1963). Favorable conditions for earthworms in the tropics include an undisturbed soil which has a regular and adequate water supply. Generally a fine soil texture is required but this is a concomitant of the physical availability of water since water will rise to a greater height in fine soils. In addition to these soil requirements, earthworms require a regular and adequate supply of organic material. Even though the layer of humus in tropical soils is very thin, earthworms can and do occur there and may be found even in the red sandy soils in the vicinity of paddy fields. Indeed, light and medium loams appear to carry higher proportions of worms than the heavier clay type soils or more gravelly sand and alluvial soil types (Guild, 1948). Local abundance of earthworms may range from 6 kilograms per acre in a maize field to 2,339 Kg/acre in an artificial forest (El-Duweini and Ghabbour, 1965).
We sampled the earthworm population in the soils composing the floor of the eucalyptus forest at Manandroy and found earthworms to be practically absent. On the other hand, earthworms did occur in the vicinity of the paddy fields and other cultivated fields. This has led us to conclude that the eucalyptus forest served as a sleeping area rather than as a primary foraging area and furthermore the animals would need to move out each night into the vicinity of the fields in order to provide themselves with sufficient earthworms.
Consumption of earthworms by captive individuals was studied in some detail. It was found that the average intake during a 15- to 20-minute feeding period to satiation for three specimens of Hemicentetes nigriceps ranged from 13.0 to 4.2 grams. The maximum intake was by an adult and the minimum by an infant. Yet the animals feed several times a day, and in order to determine average food intake for a 24-hour period, a sample of six Hemicentetes nigriceps were fed and weighed four times in each 24-hour period. This procedure was carried out for four days. The average increase in weight plus average consumption of worms for a 24-hour period could be calculated. Food intake for adults and juveniles averaged approximately 100 grams of earthworms in each 24-hour period, that is, the animal ingests approximately its own weight in worms daily. A young juvenile would tend to exhibit approximately 1.7 grams net gain in weight for each 24-hour period. This would indicate approximately 4.1 percent of the wet weight food intake was converted to net gain in weight for the animal feeding (see Figure 54).
The nutritional value of earthworms is rather high. The average dry weight of earthworms is about 15 to 20 percent of the wet weight. Protein accounts for the largest fraction of the dry weight and has been estimated between 53.5 and 71.5 percent of the total dry weight of Lumbricus terrestris. Measurements of L. rubellus and Eisenia rosea have a similar proportion of dry weight (16.38% which consists of 16.3% protein, 17% carbohydrate, 4.5% fat, with only 15% ash residue) (Laverach, 1963). The nutritional quality of earthworms is certainly adequate for rapid growth. In captivity, our H. nigriceps grew rapidly and, indeed, some question may be raised concerning the validity of our captive growth studies since we may have been feeding a diet with nutritional qualities far exceeding those in the wild. For example, total length could increase in captivity over a 30-day period by an increment of approximately 40 mm.
As we have previously stated, we had established a marked population of animals at Manandroy which were sampled in February and again in April 1966. By recaptures, we could estimate growth in the field and found that over a 2-month period a juvenile in the 104 mm age class could increase in total length some 31 to 36 mm. Larger animals first captured in the 141 to 148 mm total length class would increase in total length over the same 60-day interval by approximately 14 to 15 mm. This indicates that although we may have slightly accelerated growth in captivity, we certainly did not distort too far from the field situation since increase in total length is certainly very rapid, even under field foraging conditions.
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The Tenrecs: A Study in Mammalian Behavior and Evolution by J. F. Eisenberg & Edwin Gould, pp. 78-89.
published in Smithsonian Contributions to Zoology No. 27 (1970)
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Back to Tenrec Resources and Information