Nov 7, 1977 - Werribee, Vic., Fowlers Gap Station, N.S.W., and Willandra National Park, .... in the National Museum of Victoria, the South Australian Museum, ...
Aust. Wildl. Res., 1978, 5, 183-211
An Ecological Study of Sminthopsis crassicaudata (Marsupialia :Dasyuridae) 111". Reproduction and Life History
S. R. Morton Department of Zoology, University of Melbourne, Parkville, Vic. 3052.
Abstract Reproduction in Sminthopsis crassicaudata was studied at three sites in south-eastern Australia: Werribee, Vic., Fowlers Gap Station, N.S.W., and Willandra National Park, N.S.W. At Werribee, the breeding season covered the period July-February. Individual females attempted to raise two litters during this season; there was no significant difference between the numbers of young weaned from first and second litters. Some females bred in two seasons, but it is unlikely that any males did so. At Fowlers Gap Station, breeding occurred in the same months as at Werribee, but there was variation between years in the onset of reproduction. At Willandra National Park, breeding occurred in the period June-December. There was no evidence of unseasonal, opportunistic breeding at either of these sites. As judged by pit-trapping, populations of invertebrate animals peaked in summer at Fowlers Gap Station, and probably at Werribee. Changes in weight and fat reserves also suggest that autumn and winter were periods of depressed food supply. The adaptive significance of the double-litter system and polyoestry is discussed. It is concluded that the overall biology of S. crassicaudata reflects adaptation to a fluctuating food supply.
Introduction The most important aspects of the reproductive strategy of a small mammal are the breeding season, the number of young per litter, the number of litters produced in a season, and the number of seasons in which an individual may reproduce. This paper contains information on these characteristics in Sminthopsis crassicaudata (Gould). Of particular interest is the wide distribution of this species through mesic, semiarid and arid regions (Morton 1978a). The reproductive adaptations of Australian small mammals to arid environments are almost completely unknown, and there is very little information on breeding in any desert-dwelling insectivorous mammals. Reproduction in S. crassicaudata in the laboratory has been closely studied (Martin 1965; Ewer 1968; Godfrey 1969a; Smith and Godfrey 1970); the species contrasts with many other dasyurid marsupials in being polyoestrous. However, there has been no study of breeding in the natural situation. A major aim of the present work, therefore, was to compare reproduction in populations of S. crassicaudata in a mesic environment (Werribee, Vic.) with that in an arid environment (Fowlers Gap Station, N.S.W.); observations were also made in a semiarid habitat in central New South Wales (Willandra National Park). These study areas were described
* Part 11, Aust.
Wildl. Res., 1978, 5, 163-82.
S. R. Morton
by Morton (1978a). The emphasis of the study was on the relationship between reproduction and changes in food supply. This was achieved by a systematic survey of the abundance of terrestrial invertebrate populations over a 2-y period, in order to identify those periods of the year in which the animals' energy balance allowed successful breeding. S, crassicaudata also has a conspicuous morphological characteristic-the swollen tail containing a store of fat-which can be used to estimate states of energy balance. The fat store shrinks in animals deprived of food, whereas well fed animals have markedly thickened tails (Godfrey 1968; Ride 1970). However, apart from some preliminary studies of the structure and biochemistry of the fat stores (Sabine et al. 1968), no quantitative information is available. Thus, information on seasonal changes in the amount of fat stored in the tails of free-living S. crassicaudata, and their relation to changes in food supply and to the reproductive cycle, are also presented. Materials and Methods Assessment of' Reproductiue Condition Techniques for capture and handling have been described elsewhere (Morton 1978a; 19786). Reproductive condition was assessed as follows.
(i) Males The width of the scrotum was measured to the nearest 0.1 mm. (ii) Females The condition of the pouch was used to infer the reproductive state of females; these criteria were derived from Godfrey (19696) and Godfrey and Crowcroft (1971). Briefly, in non-parous females the pouch opening is constricted and the hair inside it is pale and dense; in contrast, the pouches of parous, oestrous or pouch-gravid females are slackened and comparatively hairless. When pouch young were present they were counted, their development was noted and the crown-rump length of one per female was measured. Laboratory Studies of Growth In order to estimate the age of pouch young and juvenile animals in the field, studies of growth in laboratory animals were carried out. Animals were bred in captivity and various measures of growth were assessed in order to provide reliable aging criteria.
(i) Maintenance of animals Glass aquaria and lacquered plywood cages with wire-screen lids, and with a layer of wood shavings on the floor, were used for the laboratory animals. Wooden nest-boxes and cardboard cylinders were provided as shelter. The cages were housed in a naturally lit room whose temperature was maintained at 22+ 3°C. Each animal was fed nightly with Harper's puppy chow and a Heinz baby food preparation with added vitamins and minerals (see Morton 1976). Mealworms, Tenebrio molitor larvae, were given when available, and field crickets, Teleogryllus commodus, were collected for food in summer. Water was always available in dishes. Animals were kept in pairs until the female became pregnant or gave birth, and then the male was removed. All births took place during August-February, and the females were examined infrequently outside this period. From August onwards their pouch condition was checked every 2-3 days until they became pregnant. Animals from three localities were maintained, but individuals were not cross-paired; the localities were Werribee, Fowlers Gap, and Stanhope, Vic. (36"24'S., 145"OO'E.). (ii) Growth studies The date of birth of young was determined by checking the mother's pouch daily until parturition. Following this, the crown-rump length of one of the young was measured every 1-2 weeks, and the
Ecology of Sminthopsis cvassicaudata. I11
gross appearance of the young noted, until they reached the age of 50 days. At this time the eyes of the young opened and they became more mobile. Subsequently, measurements of pes length, tail length, weight, and the scrotum width of males were taken every 2-4 weeks until the animals became adult. Animals from Werribee consistently failed to breed in captivity, and therefore four pregnant females were brought from the field into the laboratory in the breeding seasons of 1974 and 1975. Two of these females successfully raised their litters.
Variation in Nipple Number As part of a study of geographic variation in S, crassicaudata, all spirit specimens of this species in the National Museum of Victoria, the South Australian Museum, the Western Australian Museum, the Australian Museum and the Queensland Museum were examined. Nipple number was ascertained on as many females as possible from these collections. Unfortunately, the pouch of non-breeding females is usually hairy and has a constricted opening, and it is very difficult to count the nipples of such animals. Hence, the number was ascertained only from females with young.
Studies of Fat Storage Each animal captured was weighed to the nearest 0.1 g, the width of its tail at the point of maximum incrassation measured to the nearest 0 . 1 mm, and the length of the tail from the beginning of incrassation measured to the nearest millimetre. Field studies of variation in fat storage were supplemented by laboratory analysis of the amount of fat present in caudal and body fat deposits. S. crassicaudata were weighed, killed, and frozen until analysis. The tail was cut from the body, measured and weighed, and cut into sections approximately 5 mm thick. It was then treated with ether in a Soxhlet apparatus for 50 h. The tail residue and the flask containing the fat were weighed after at least 24 h in a 50°C oven. The body was cut transversely in half, and each section was treated as above for approximately 100 h. The remains of the body and the flask containing the fat were weighed after at least 48 h in the oven. The tails of six S. cvassicaudata from Werribee and of three from Fowlers Gap, and the bodies of three from each locality, were analysed.
Diet Analysis of the stomach contents of four S. cvassicaudata captured during the night at Werribee showed that quantitative assessment of prey items was impossible because the material was so highly triturated. Study of the diet was therefore restricted to the more easily collected faeces. At Werribee, nest sites of S . cvassicaudata usually contained faecal accumulations; freshly deposited faeces were collected from these, and also directly from animals, during 1973 and 1974. At Fowlers Gap, faeces were collected from animals after capture and frozen until analysis. Before examination, faeces were dried and then lightly crushed with a mortar and pestle, floated on water in a thin layer, and scanned under a binocular microscope. Recognizable insect remains-usually leg-parts, antennae and mandibles-were removed and identified by comparison with specimens of the possible prey items. Extensive collections of prey items were available from pit-trapping studies described below.
Seasonal Changes in Insect Abundance The abundance of terrestrial invertebrates was gauged by periodical pit-trapping. Glass jars 15 cm deep, with mouths 8.5 cm in diameter, were buried so that their openings were flush with the soil surface. A saturated solution of picric acid was added to each jar to a depth of about 10 cm. At Werribee, 20 jars were buried in a line at intervals of 4 m in an area of sparse, embedded rock 0.5 km north of the study sites. After 7 days the jars were brought to the laboratory where the insects were sieved from the picric acid. Pit-trapping was carried out at intervals of 2-3 months from June 1974 to May 1976. At Fowlers Gap, 50 jars were buried in a line at intervals of 5 m on plains country adjacent to the main study sites. After 3-5 days they were brought to the laboratory and the contents sieved. During summer the preservative had to be replenished every day to counter evaporation. Pittrapping was carried out at intervals of 2-3 months between October 1973 and November 1975.
S. R. Morton
After being sieved, insect samples were stored in 70% alcohol until analysis. Each sample was sorted into species, and each species assigned an approximate dry weight. The number of specimens of each species in a sample was multiplied by the appropriate weight, and the sum of these products gave an estimate of biomass. This estimate was standardized to biomass per pit-trap per day. Ants (Formicidae) were abundant in all samples, but because they did not appear to be important constituents of the diet of S. crassicaudata, they were excluded to simplify the analysis.
Fig. 1. Semilogarithmic relationship between crown-rump length and age of pouch young of S. crassicaudata in the laboratory. Calculated regression line (see text) and 95% confidence limits also shown.
Fig. 2. Relationship between age and scrotum width of male S. crassicaudata in the laboratory. Calculated regression line for ages 50-160 days, and 95 % confidence limits, also shown.
Results Criteria for Aging (i) Pouch young The crown-rump lengths of young aged from 0 to 50 days are plotted on a semilogarithmic scale in Fig. 1. The number of litters from which measurements were taken was eight: four from Stanhope animals and two each from Fowlers Gap and Werribee animals. A regression line fitted to these data has the equation: logy = O.O196x+O-6353,
(1)
where y is the crown-rump length in millimetres and x is age in days. Since this relationship was to be used for inverse prediction, i.e, the independent variable x (age) was to be estimated from the dependent variable y (crown-rump length), appropriate confidence limits were calculated according to Sokal and Rohlf (1969, p. 446).
Ecology of Sminthopsis cvassicaudata. I11
(ii) Scrotum width in males The only measurement found to predict the age of juvenile S. crassicaudata accurately over a sufficiently lengthy time-span was the scrotum width of males. This increased in size in a predictable manner up to the age of 170 days (Fig. 2), i.e. approximately 100 days after weaning. The measurements were obtained from 17 males from six litters, four from Stanhope animals and one each from Fowlers Gap and Werribee animals. A regression line fitted to the data from ages 50 to 160 days has the equation :
where y is scrotum width in millimetres and x is age in days. Confidence limits were calculated for inverse prediction as described above.
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Fig. 3. Percentages of female S. cvassicaudata in four reproductive categories throughout the year at Werribee. Data for four years pooled. Juveniles of the year shown separately from adults for October-March. Solid blocks, females pregnant or suckling young; vertical lines, parous adults neither pregnant nor suckling; open blocks, non-parous adults; horizontal lines, juveniles. Numerals on graph, sample sizes.
(iii) Information on growth in thefield At Werribee, some females were caught twice with the same pouch-litter and some juvenile males were also caught twice. Measurements taken at each capture enabled two calculations of the age of the young, and provided a test of the validity of the laboratory growth data. In six litters of pouch young, the ages were underestimated at the second capture by 1-5 days. This information suggests that growth was marginally slower in the field than in the laboratory, but the discrepancies were within the confidence limits of equation 1. In six juvenile males, discrepancies in calculated age at the second capture varied from an overestimate of 10 days to an underestimate of 29 days. The latter record was the only one that fell outside the confidence limits of equation 2. These data confirm that growth of captive S. crassicaudata (particularly pouch young) is similar to that of free-living animals.
S. R. Morton
Reproduction at Werribee (i) Breeding season The percentage of females at Werribee in four different reproductive categories throughout the year is shown in Fig. 3. It can be seen that females with young were found in all months from July to April. One pouch young from each female was measured, and the date of birth calculated with equation 1. This provided sufficient data to interpret the reproductive cycle, and it was not necessary to calculate the ages of juvenile males. The numbers of individual litters born in half-monthly periods of the year, as derived from calculation of the age of pouch young, are given in Fig. 4. Births took place from the third week of July until the last week of February; no evidence of births in other months was found. The gestation period of S. crassicaudata is 13 days (Godfrey and Crowcroft 1971); hence the breeding season [i.e. period of female conception (Sadleir 1969)l is from the first week of July until the second week of February. Females care for their young for approximately 70 days after birth (Godfrey and Crowcroft 1971). Fig. 5
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Fig. 4. Numbers of litters of S, crassicauduta born in half-monthly periods at Werribee. Dates of birth calculated from the size of pouch young and unweaned young. No young were born during March-June. Date from four years pooled. Fig. 5. Percentages of female S. crassicaudata in three reproductive categories throughout the breeding season at Werribee. Data for four years pooled. Juveniles of the year excluded. Solid blocks, females pregnant, suckling young or having weaned their first litters; hatched blocks, females neither pregnant nor suckling their first litters, but whose pouches indicate oestrus or recent oestrus; open blocks, females not yet in oestrus. Numerals on graph, sample sizes.
No evidence of variation in the timing of reproduction from year to year was observed, and the data for each year of study were pooled for the above analysis. (ii) Number of litters raised by individual females during the breeding season There was considerable variation in the timing of reproduction among individual females (Fig. 3); even though reproduction began in July, females that were neither pregnant nor suckling were found until October, and recaptures of one unusual female showed that she did not give birth to her first litter until early December.
Eco!ogy of Sminthopsis crassicaudata. I11
A large proportion of the females found from August to October that were neither pregnant nor suckling were either in oestrus or had recently experienced oestrus without becoming pregnant (Fig. 5). If a female failed to conceive at the first oestrus, she could not become pregnant again for at least another 4 weeks because the length of the oestrous cycle in S. crassicaudata is, on average, 31 days (Godfrey and Crowcroft 1971). Hence, much of the variation in the timing of births evident in Fig. 4 is apparently due to failure to conceive at the first oestrus; nevertheless, Fig. 5 shows that some females did not undergo oestrus until September. Because of the continual movements of the animals (Morton 1978b), few females were recaptured over a sufficient period of time to permit a complete interpretation of their reproductive cycle. Details of the sequence of litters in nine females that were recaptured throughout the breeding season showed that their first litters were born in the period from late July until early October, the only exception being the female mentioned above, that did not give birth until early December (this female was not captured in October or November, and hence does not appear in these months in Table 1. Changes in litter size with litter age in S. crassicaudata at Werribee
Data for 1972-76 pooled. At 50-70 days old, values for first and second litters given separately as well as together Age class (days) 0-9 10-19 20-29 30-49 50-70 1st 2nd
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7.5 7.3 6.1 5.8
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Fig. 5). Following their first litters, these females gave birth to second litters during the period from early November to late February. The one exception was a female whose second litter was born in early October, but the birth of the first litter of this female was also unusually early (late July). Only two females were recaptured after weaning of their second litter; neither of these showed evidence of further reproduction. Full details of these animals are provided in Morton (1976). Thus the data in Fig. 4 can be interpreted as follows. It is almost certain that litters born up until the middle of October were first litters, with one known exception. Since all the females captured were breeding by the end of October (Fig. 5), it is probable that all litters born after this time were second litters (again, there was one known exception). Therefore the two peaks in numbers of litters born (in August and December-January) (Fig. 4) represent concentrations of first and second litters respectively. The spread of birth-dates was greater during the period of second litters than in that of first litters, but was probably a result of failure to conceive at oestrus as described above. The variation in birth-dates of the first litters would accentuate variation due to the same cause throughout the second-litter period.
S. R. Morton
Although second litters were born over a greater period of time, the number observep (34) was not markedly less than the number of first litters observed (43). In captivity, some S, crassicaudata may produce three consecutive litters (Ewer 1968; Godfrey and Crowcroft 1971). In the present study, the breeding season was shown to be long enough for three consecutive litters to be raised in the field. However, no evidence was found of females producing three litters in one breeding season. Similarly, although female S. crassicaudata in captivity are capable of breeding at an age of 160 days (Godfrey and Crowcroft 1971), there was no evidence that any female in the field reproduced in the season of her birth.
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Fig. 6. Mean monthly weights of S. cvassicaudata at Werribee. (a) Males. (b) Females. Juveniles (m) distinguished from adults ( @ ) until the April following their birth. Unweaned young excluded. Data for four years pooled. Numerals on graphs, sample sizes. Means and 95 % confidence limits are given for samples of five or more; means and ranges for smaller samples.
(iii) Litter size and number of young weaned Data on changes in litter size from birth to weaning are presented in Table 1. Litters were aged according to the criteria described above, and grouped into five age classes.
Ecology of Sminthopsis crassicaudata. I11
Although most females at Werribee probably have 10 nipples (see below), the average litter size at birth was 7.5. Two females were accidentally killed while pregnant; one of these contained 10 and the other seven foetuses. There was a gradual reduction in the size of the litters with age, and the mean number of young weaned was approximately 5.4. There was no significant difference between the numbers of young weaned from first and second litters. (iv) Population structure Females. Fig. 3 shows that during the non-breeding period the population contained two groups of females: parous and non-parous adults. In the months of May-July, parous adults comprised 23 % of the females in the population. Very few of these, however, were known to reproduce in a second breeding season; details of the reproduction of three such females are given in Morton (1976). It is therefore very unlikely that any females live for more than 2 y, and most appear to live for less than 18 months.
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Fig. 7. Mean monthly weights of S. crassicaudata in four non-breeding periods at Werribee. (a) Females. (b) Males. Unweaned young excluded from 1973. the values for April. o 1972. 1974. 1975.
Months
Males. The situation in males was more difficult to determine. From April onwards, I-y-old males could not be differentiated from males born during the breeding season, since their scrotum widths became similar during this period. In addition, their extensive movements [possibly greater in males than in females (Morton 1978b)], resulted in few recaptures. The small number of males captured in January-March, however, suggests that adult males become uncommon late in the breeding season. Table 2 shows that the adult sex ratio of the population varied significantly from unity only in January-March. The sex ratio of juveniles did not differ significantly from unity in this period. These data suggest that few males survive longer than 15 or 16 months. (v) Changes in weight Average monthly weights of males and females are shown in Fig. 6. Females grew little in May and June, and then gradually increased in weight in July and August
S. R. Morton
as they began to breed. Males also showed this halt in growth early in winter, but in July showed a significant increase in weight to a level that was maintained throughout the breeding season. In May and June the weights of males did not differ significantly from those of females. However, in July and August males were significantly heavier (t-test: July, P < 0.001; August, P < 0.001). Males also showed significant year-to-year variation in winter weight in every month (Fig. 7, Ptest: April and May, P < 0.001 ; June, P < 0.005; July, P < 0.025), whereas in females none of the variation was significant.
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Fig. 8. Mean monthly maximum tail widths of S. crassicaudata at Werribee. (a) Females. (b) Males. Data from four years pooled. Numerals on graph, sample sizes. Vertical lines, 95 %confidence limits. Table 2. Male and female S. crassicaudata captured in 3-monthly periods at Werribee
Data for 1972-76 pooled. Unweaned young excluded. (P i0.001)from 1 : 1 ratio
Numbers Adult male Adult female Juvenile male Juvenile female Sex ratio (M : F) Adult Juvenile
* Differs significantly
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(vi) Changes in fat reserves Seasonal changes in maximum tail width are shown in Fig. 8. In both males and females, tail width rose to a peak in May and then decreased to the lowest values in November-February. Analysis of variance of the means showed that the monthly changes in both males and females were significant (I;-test: males, P < 0-001;
Ecology of Sminthopsis crassicaudata. I11
females, P < 0.001). Further, the mean maximum tail widths of males were consistently greater than those of females, and this difference was significant throughout the year (Mann-Whitney U-test: P < 0.05). Tail width in males showed an increase from June to July, corresponding to the increase in weight over this period (see Fig. 6). The above analysis does not allow for the possibility that seasonal trends in fat storage were obscured by the changing age structure of the population. Juveniles comprise most of the population from January to April (Table 2), and because they are smaller and have shorter tails, analysis of the absolute values of maximum tail width may obscure changes in the relative amounts of fat stored by juveniles and adults. Hence, all the data used in Fig. 8 were transformed by dividing tail length into tail width to create a relative estimate of fat storage. These data then were averaged by month and compared with Fig. 8. The same trends emerged, and it was concluded that the absolute values accurately reflected the seasonal changes in fat storage.
Fig. 9. Numbers of litters of S. crassicaudata born in half-monthly periods at Fowlers Gap. Hatched blocks, birth dates calculated from size of pouch young; solid blocks, birth dates calculated from scrotum width of juvenile males.
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Reproduction at Fowlers Gap (i) Breeding season Birth dates were calculated for each litter of pouch young and for each juvenile male whose scrotum width was less than 7 mm, and the distribution of these birth dates is shown in Fig. 9. It should be borne in mind that birth dates calculated from scrotum width are less accurate than those calculated from crown-rump length of pouch young. Further, it is possible that more than one juvenile male from a single litter was captured and aged, so that this litter is over-represented in Fig. 9. However, in view of the very low recapture rate of individuals at this site (Morton 1978b), it seems likely that the probability of such over-representation is very low. The results show that S. crassicaudata bred within the same period as at Werribee, i.e. July-February. However, there was variation in the onset of breeding from year to year. Breeding began in the July of 1973, but in both 1974 and 1975 there was no evidence of reproduction before September, and non-breeding females were caught
S. R. Morton
in August in both these years. Unfortunately, few animals were caught in the latter half of 1975 and early 1976, but the evidence suggests that the same breeding pattern occurred as in the previous years. It was possible to determine the sequence of litters in only one female from this population. She was captured in October 1974 with pouch young aged 26 days, and recaptured in December 1974 with a litter aged less than 1 week; thus she had produced two litters. The spread of litters in each breeding season (Fig. 9) was also consistent with the situation described for the Werribee population.
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Fig. 10. Mean weights of S. crassicnudata at Fowlers Gap in each sampling period. (a) Males. (b) Females. Numerals on graphs, sample sizes. Means and 95% confidence limits are given for samples of five or more; means and ranges for smaller samples.
Insufficient data were obtained on litter size and population structure to enable comparisons to be made with the Werribee population. (ii) Changes in weight Mean weights of males and females captured in each sampling period are given in Fig. 10. Although data are sparse, there was a general trend for weight to increase
Ecology of Sininthopsis crassicaudata. I11
from the beginning of each year until the beginning of the breeding season (about August); after this, juveniles entered the population and mean weights were lower. It is difficult to determine whether there was a halt in growth during winter, as was evident at Werribee, but two facts suggest that there was. First, the weight of males increased from June to August in 1974, indicating that they weighed less during winter. Second, the weight of females decreased from May to August in 1975, even though no juveniles were present in the latter sample. Another similarity with the pattern at Werribee Iies in the onset of sexual dimorphism in weight. Two samples during May, a non-breeding period, showed males (11.9 g) to be almost the same weight as females (12.0 g), but three samples in August, at the beginning of the breeding season, showed males (14.5 g) to be significantly heavier than females (1 1.4 g) (t-test: P < 0.001).
Fig. 11. Mean maximum tail widths of S. crassicaudata at Fowlers Gap in each sampling period. ( a ) Females. (b) Males. Numerals on graphs, sample sizes. Means and 95 % confidence limits are given for samples of five or more; means and ranges for smaller samples.
(iii) Changes in fat reserves Mean maximum tail widths for males and females at each sampling period are shown in Fig. 11. Although the samples were taken at irregular intervals and were sometimes small, the trend observed at Werribee seemed to be present here, i.e. decreased fat storage throughout the breeding season, a peak in autumn, and then a decrease again throughout the winter and the subsequent breeding season. In samples of four or more, males had significantly thicker tails than females (MannWhitney U-test: P < 0.05). Reproduction at Willandra (i) Breeding season Calculated birth dates for each litter of pouch young and for each juvenile male whose scrotum width was less than 7 mm (Fig. 12) show that the breeding season was from June until December, i.e. 1-2 months earlier than at Werribee or Fowlers Gap.
S. R. Morton
No females were recaptured, but the spread of litters suggests that at least two were produced by each female. The mean size of seven litters whose calculated age was 10 days or less was 8.1 (range 7-9). 6
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Fig. 12. Numbers of litters of S. crassicaudata born in half-monthly periods at Willandra in 1972-73. Hatched blocks, birth dates calculated from size of pouch young; solid blocks, birth dates calculated from scrotum width of juveniles.
Fig. 13. Relationship between the mass of fat extracted from tails of S. crassicaudata and the estimated volume of the tails (considered to be cone-shaped). Calculated regression line (see text) also shown.
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(ii) C h a ~ g e sin weight and fat reserves Mean weights and maximum tail widths of males and females captured in each sampling period are given in Table 3. There were insufficient data to determine whether seasonal trends in weight were similar to those demonstrated at Werribee. However, sexual differences in weight changes were evident. In late May 1973, just before the beginning of breeding, males were significantly heavier than females (t-test: P < 0.001), whereas in April 1973 the difference, slightly in favour of mkles, was not statistically significant. Although the period of study at this site was short, the tail widths of both males and-females showed a peak just before breeding (May) and a decrease during breeding.
Ecology of Sminthopsis crassicaudata. I11
Variation in Nipple Number Nipple numbers of 66 females are shown in Table 4. Populations did not appear to differ in nipple number, and the number varied among females from the same localities. The data do suggest, however, that the nipple number may be more variable in northern populations. Both the extremes-1 1 (South Australian Museum, S3490) and six (National Museum of Victoria, C4791)-were found in females from the Northern Territory; the unusual latter record was probably the female described by Spencer (1896). Table 3. Weights and tail widths of S. crassicaudata at Willandra in 1973 In June and November females carrying pouch young are excluded Month Apr.
M F
May
M F
June
M F
NOV.
N
Weight (g) Mean
22 15 17 15 6 6 5
14.5 13.2 17.8 14.6 19.6 16.7 11.6
Sex
M F
-
Maximum tail width (mm) N Mean SE
SE
22 15 17 15 6 12 5 5
0.6 0.7 0.5 0.5 1.3 0.7 1.8 -
-
4.7 4.4 4.9 4.7 4.3 4.1 3.6 4.1
0.2 0.2 0.1 0.2 0.2 0.1 0.2 0.2
Table 4. Numbers of museum specimens of S. crassicaudata with different numbers of nipples, by latitude Latitude
(3 23 24 25 26 27, 28 29 30 31 32 33 34 35 36 37 38
West. Aust. 9
10
6
S. Aust. and N.T. 7 8 9 1 0 1 1
Qld, N.S.W., Vic. 8
9
10 2
3
1 2
1 1 1
2 1 1
1
4
1 1
2 2 1
1
2
1 3
2
1
1 1 1
1 3 3 1 2 3 1 2 11
The majority of females examined had 10 nipples, but litters of eight or less. The nipples not used were invariably the posterior pair, which were usually tiny and undeveloped. Laboratory Studies of Fat Storage In Fig. 13 the mass of fat extracted from the tail is plotted against the volume of the tail; the latter was calculated by assuming the tail to be a cone, thus taking into account the fact that both thicker and longer tails contain more fat. The length
S. R. Morton
of the tail was measured from the beginning of the incrassation, about 4 mm from the origin of the tail, to the tip. The tails of S. crassicaudata from Fowlers Gap were longer than those of Werribee animals, and the three greatest volumes in Fig. 13 represent the specimens from this locality. A regression line fitted to the data points has the equation: y = 0 . 0 0 1 9 ~ -0.0772, where y is the mass of fat in the tail in grams and xis the volume of the tail in cubic millimetres. Fat comprised 44.8 f 16.0% (standard deviation) (n = 9) of the wet weight of the tail. Table 5. Amount of fat present in the body of 5'. crassicaudata of two populations Population
Sex
Weight (g)
Werribee Werribee Werribee Fowlers Gap Fowlers Gap Fowlers Gap A
M M FA M F F
16.0 14.2 18.1 16.5 10.6 9.1
Amount of fat Mass (g) % 0.801 0.520 3.330 0.614 1.233 0.862
5.0 3.7 18.4 3.7 11.6 9.5
Lactating.
Results of extraction of fat from the bodies of S. crassicaudata are presented in Table 5. The average mass of fat, excluding the figure for the lactating female, was 0.806 g, and the average proportion of fat in the total body weight was 6.7 %.
Geographical Variation in Tail Length and Body Weight (i) Tail length The length of the tail of S. crassicaudata varies geographically, being least in individuals from southern populations and gradually increasing in more northerly populations (Spencer 1896; Thomas 1902; Finlayson 1933; Troughton 1964; Hope and Godfrey 1968; Archer 1978; Morton, unpublished data). Table 6 Table 6. Variation in length of incrassated tail in three populations of S. crassicaudata Population
N
Mean tail length (mm)
Coefficient of variation (%)
Variance
Werribee Fowlers Gap Willandra
136 136 77
34.7 52.3 50.1
6.3 6.5 5.2
4.8 P < 0.001 11'6 P < 0.02 6.6
summarizes information on adult tail length in the three populations studied; all the information available from Willandra and Fowlers Gap is presented, but a random sample from the four years of measurements at Werribee has been used. The data show that in S. crassicaudata from Fowlers Gap, tail length was both greater and more variable than in animals from either Werribee or Willandra. Although animals from Willandra had longer tails than those from Werribee, they were not significantly more variable in tail length. Thus tail length of S. crassicaudata was most variable in the most arid environment:
Ecology of Sminthopsis crassicaudata. I11
The differences in tail length were accompanied by variation in the amount of incrassation seen in free-living animals. The tails of S. crassicaudata from Fowlers Gap and Willandra were often over 5 mm in maximum thickness, but throughout the study only six animals from Werribee were observed to have tails of this thickness (see Figs 8, 11 ; Table 3). Animals from more arid regions, therefore, have a greater capacity for tail incrassation. (ii) Body weight Table 7 shows that S. crassicaudata from Werribee and Willandra weighed 2-3 g (about 15%) more than those from the most arid population (Fowlers Gap); these differences were significant (Werribee compared with Fowlers Gap, t-tests: males, P < 0.001; females, P < 0.001). This difference in weight is not accompanied by a change in size, since head and body length remains constant throughout the range of S. crassicaudata (Morton, unpublished data). Table 7. Body weights in three populations of S. crassicaudata Population
Breeding males N Wt (g)
Breeding females N Wt (g) -
Werribee Willandra Fowlers Gap
22 17 24
17.6 17.8 14.5
Non-breeding males N Wt (g)
Non-breeding females N Wt (g)
-
16 15 15
15.5 14.6 11.4
53 22 23
13.6 14.5 11.9
37 15 9
12.6 13.2 12.0
Diet Results of analysis of faeces are presented in Tables 8 and 9. There are several cautionary points to be made. (1) Some remains were easily recognizable or persistent because of their strength, e.g. the leg parts of curculionid beetles and spiders, whereas others were easily overlooked. (2) Not all possible prey items have structures which would appear in the faeces. For example, earthworms (Lumbricidae) were found in the stomach contents examined in 1972, but were not recorded in faecal material. (3) Some prey are probably dismembered before being eaten, and legs and mouthparts may therefore not appear in the faeces. Nests discovered at Werribee often contained accumulations of elytra of the field cricket Teleogryllus commodus, legparts and wings of acridid grasshoppers, legparts and elytra of the scarabaeid beetle Rhopaea heterodactyla, and on one occasion the wings of a large dragonfly (Odonata). At Fowlers Gap in August 1972, an animal was chased into a hole containing many wings of small moths. Nevertheless, some qualitative conclusions can be drawn. First, although the range of invertebrates eaten by S. crassicaudata was large, certain groups were poorly represented in faeces even though their remains are conspicuous. Cockroaches (Blattodea) and slaters (Isopoda) were absent, and ants (Formicidae) were found infrequently and most often in winter. Second, spiders appear to be an important year-round food source. Third, vertebrates are rarely eaten. The vertebrate bones found were very finely splintered and could not be identified, but, in view of the absence of hair in the faeces, it seems most likely that they were from frogs or reptiles
S. R. Morton
A
0.1
I 1
2 1
1
1
May
1-1973-,
0.1
1
1
1
Aug.
Remains consisting of finely splintered bones.
Mass of faeces (g)
Chilopoda Dermaptera Orthoptera
Scolopendromorpha Unidentified Gryllidae Acrididae Hemiptera Cicadellidae Lygaeidae Pentatomidae Unidentified Heteroptera Coleoptera Carabidae Staphylinidae Scarabaeidae Elateridae Curculionidae Unidentified Larvae Larvae Lepidoptera Hymenoptera Formicidae Araneida Unidentified VertebrataA
Prey
Table 9. Prey items found in faeces of S. crassicaudata from Fowlers Gap
0.1
Oct.
0.25
Nov.
0.1
Jan.
,
0.1
Mar.
1974 3-
0.15
June
0.1
Aug.
0.15
Oct.
0.1
Dec.
Values are of the minimum number of species represented in each taxonomic group
0-2
Feb.
-1,975-,
0-4
May
0.1
Aug.
0.2
Nov.
S. R. Morton
rather than from mammals. Fourth, some seeds and other vegetable material were present, but seeds were usually undigested. S , crassicaudata is therefore almost completely insectivorous.
Seasonal Changes in Insect Abundance Changes in invertebrate biomass derived from pit-trap collections at Fowlers Gap are shown in Fig. 14. There was a clear trend of increased food availability in summer and decreased availability in winter. These results suggest that invertebrates are not abundant until late spring (November), but this is discussed more fully below. Although nearly every month of 1973 and 1974 had above-average rainfall (Morton 1978a), there was no evidence that this led to any winter peaks in insect abundance or activity. The food supply of S, crassicaudata in this habitat is therefore distinctly seasonal.
Fig. 14. Seasonal changes in the abundance of terrestrial invertebrates at Fowlers Gap, as determined by pit-trap sampling.
Changes in invertebrate biomass at Werribee did not show a consistent seasonal trend, and there was more variation between years, in comparison with the samples from Fowlers Gap. Two factors may have increased variability between samples at Werribee. First, the smaller number of pit-traps used could have resulted in poor sampling. Second, the invertebrate fauna at Werribee appeared to be less diverse than that at Fowlers Gap (the number of species sampled at Werribee was 45; at Fowlers Gap, 80), and in this case a single species may dominate during a sampling period. For example, at Werribee in July 1974 rain fell during most of the sampling period, and earthworms constituted 86 % of the measured biomass (Morton 1976). A further problem, which also applies to results from Fowlers Gap, was the failure of the pit-traps to adequately sample populations of grasshoppers, even though they were abundant in every spring and summer of the study at both sampling sites. It seems likely that if the biomass of grasshoppers could have been assessed, the sampling at Werribee would have shown a similar trend to that at Fowlers Gap. Distinct seasonality is known in northern-hemisphere cool-grassland invertebrates (e.g. Evans and Murdoch 1968; Van Hook 1971; Dondale et al. 1972; Janzen and Pond 1975), and it is probable that it also occurs at Werribee. It will be assumed, therefore, that the food supply for S. crassicaudata in this habitat increases in spring and summer.
Ecology of Srninthopsis cvassicaudata. I11
Detailed investigations of pit-trapping (Williams 1959; Duffey 1962; Mitchell 1963; Greenslade 1964; Ahearn 1971 ; Greenslade and Greenslade 1971 ; Luff 1975) have shown that it is of use only for measuring changes in behaviour and abundance of invertebrates within a particular habitat. Since the aim of the present study was the measurement of seasonal changes in activity and abundance of terrestrial invertebrates, it seems safe to assume that the changes shown in Fig. 14 are qualitatively valid.
Discussion Reproduction Several laboratory studies have established that S , crassicaudata females are polyoestrous and are capable of rearing at least two litters in succession (Martin 1965; Ewer 1968; Godfrey and Crowcroft 1971), but reproduction and the significance of polyoestry in the natural situation has remained unknown. Martin (1965) and Ewer (1968) suggested that polyoestry conferred the ability to reproduce continuously when conditions were suitable, and postulated that breeding was opportunistic in the wild, i.e. responded to irregular environmental occurrences such as rainfall rather than to regular seasonal events such as photoperiod or temperature. TyndaleBiscoe (1973) also speculated that S, crassicaudata may breed opportunistically at any time of the year. However, Godfrey and Crowcroft (1971), reviewing information on laboratory studies of this species, showed that over 90% of litters were born between July and February, and concluded that breeding was probably seasonal in the field. This conclusion is strongly supported by experimental stimulation of oestrus with increased photoperiod (Godfrey 1969a; Smith, personal communication), a result which indicates that daylength is an important factor in the onset of breeding. The present study has shown that breeding is seasonal in three habitats ranging from mesic grassland to arid grassland-shrubland. The available evidence indicates that only two litters are produced by each female during the breeding season in Victoria, and circumstantial evidence suggests that the same is true in central and western New South Wales. Although it is still possible that reproduction is opportunistic in more arid regions of Australia, the available information indicates that seasonal breeding is universal in this species. Spencer (1896) collected many S. crassicaudata in southern areas of the Northern Territory, but found females with pouch young only in August, November and December. Watts and Aslin (1974) observed pouch young only in spring months in north-eastern South Australia and south-western Queensland. Finally, Philpott and Smyth (1967) found no reproduction in June, July or August in S. crassicaudata from northern South Australia, even though recent rains had stimulated breeding in several sympatric species of rodents; they concluded that breeding in S. cvassicaudata was probably regular and seasonal. Further evidence favouring the above interpretation of breeding in S. crassicaudata in arid environments is derived from the rainfall pattern at Fowlers Gap through this study. During the autumn of both 1973 and 1974 heavy rainfall caused considerable growth of vegetation (Morton 1978a), but in neither year did S. crassicaudata begin to breed until July or later. Although breeding began earlier in 1973, conceivably in response to the heavy rainfall, it did not begin early in 1974 even though 120 mm of rain fell in May. If breeding were opportunistic, then the unusually heavy rainfall of these two years should have stimulated it, and it therefore seems most unlikely that S. crassicaudata would ever breed in autumn. Reasons for the lability in the
S.
R. Morton
timing of breeding at Fowlers Gap are unknown, but they may relate to the nutritional state of the animals during the winter. The present study has provided no information on the reproductive response of S. crassicaudata to prolonged drought in arid regions, and it is possible that breeding is delayed then. However, the life-span of the animals is short (18 months), and such a response would be of only limited adaptive value. They probably attempt to breed during spring and summer regardless of the conditions. The stimulus for breeding is almost certainly a regular seasonal phenomenon. Of the two potential stimuli-photoperiod and temperature (Sadleir 1969)-the former seems more probable, since oestrus in S. crassicaudata can be stimulated by increasing the daylength (Godfrey 1 9 6 9 ~ ; Smith, personal communication). Further, it is difficult to understand how temperature could provide as regular a cue as is implied by the timing of breeding at Werribee. Light is known to affect ovarian cycles and oestrus in many species of mammals (Sadleir 1969), and it seems reasonable to postulate that this is the environmental cue utilized by S. crassicaudata. The ultimate cause of the timing of the breeding season (i.e, the evolutionary cause) is the change in abundance or availability of food throughout the year. In the present study, attempts were made to gather quantitative data on seasonal changes in the food supply of S. crassicaudata in order to identify the optimal breeding period. It seems probable that in both habitats terrestrial invertebrates were most abundant in summer and early autumn, but the sampling technique failed to assess populations of acridids, an important food source for S. crassicaudata. If the acridid populations were included in the estimates of biomass, insect abundance in spring would appear much greater; nevertheless, there would still be peaks in summer because acridids appeared to be present in comparable numbers throughout both spring and summer. Food supply is therefore distinctly seasonal, increasing from a low point in winter to a peak in summer. The general correlation of the breeding seasons at Werribee and Fowlers Gap with the period of greatest food availability is clear. Reasons for the shift in breeding season at Willandra are unknown, but it seems likely that in some regions insect numbers may peak in spring rather than in summer; in this case the breeding season of S. crassicaudata may be advanced by 1 or 2 months. It is also possible that breeding may be earlier in northern Victoria than at Werribee, since a female with pouch young estimated to have been born in the second week of July was captured near Patchewollock (35"24'S., 142'12'E.) in 1973 (Morton, unpublished data). Other data support the interpretation that autumn and winter are periods of depressed food supply for S, crassicaudata. First, changes in average monthly weights at Werribee show a brief plateau or decrease in May and June; these pauses in growth also occur in another dasyurid, Antechinus stuartii (Wood 1970), and in the shrew Sorex araneus (Shillito 1963). Males, however, showed a weight gain of over 4 g during July (Fig. 6). This rapid increase, which is probably due to behavioural and endocrinological changes associated with preparation for breeding, also occurs in A . stuartii. However, the year-to-year variation in weights of males (Fig. 7) during winter suggests that variability in food supply affected males more than females. The former may be the more active at night in this season (Morton 1978b), and the variability in their weight may reflect greater variability in food supply during winter. Second, caudal fat storage showed a decline in winter. At Werribee, the amount of tail fat was greatest in late autumn, and did not rise in spring and summer; less
Ecology of Srninthopsis cvassicaudata. I11
complete observations indicated that similar changes took place in populations in more arid regions. It seems probable, therefore, that when food is more abundant in spring and summer energy is channelled into reproduction rather than fat storage. Such an effect was obvious in females; during the breeding season they invariably had thin, shrunken tails. The cause of depletion of tail fat in males in this period was presumably the increased activity associated with location and monopolization of oestrous females. Consistent differences between males and females in caudal fat storage outside the breeding season may also be related to the greater activity of males (Morton 19783). Further, juvenile animals seldom had greatly incrassated tails, and probably did not begin to store much fat until they had reached adult size. Hence, although caudal fat storage diminished during spring and summer, it peaked in autumn (when breeding had ceased and insects were still relatively abundant) and then declined throughout the winter. These results are consistent with a depressed food supply during the winter. Third, other characteristics suggest that winter is a period of stress for S. crassicaudata. Nest-sharing, a form of behavioural energy conservation, occurs most frequently at Werribee during autumn and winter (Morton 1978b, 1978~). Torpor, a physiological method of energy conservation, was observed at Werribee only during April-October, and was most common in the winter months (Morton 1978~).Low temperatures may also elicit both of these responses. The general timing of breeding in S. crassicaudata is explicable in terms of changes in food supply. The production of two litters, however, appears to be a safeguard against unpredictable variations in the timing and extent of the regular seasonal increase in insect abundance (Morton 19783). Although insects become more active and abundant in summer, the amount of increase is variable because of the effect of various climatic factors on grassland or desert insect populations. Thus there is a dependable increase in food supply in summer, but the precise timing and amount of the increase are not predictable. In these circumstances natural selection has favoured more than one attempt at breeding; if one litter survives poorly, then a second may improve the female's overall reproductive success. The mean sizes of the first and second litters weaned at Werribee were not significantly different (Table I), but variation among these litters was considerable. Similar variation is almost certain in other populations of this species; a female was captured at Willandra in November 1973 with only one pouch young. Polyoestry in S. crassicaudata, therefore, has probably evolved as a response to the variability of its food supply. The seasonal breeding shown by S, crassicaudata contrasts with some other mammals of semiarid and arid regions. In Australia the best known opportunistically breeding mammals are the red kangaroo Megaleia rufa and the euro Macropus robustus (see reviews by Newsome 1971, 1975), but it is almost certain that many of the native rodents also breed opportunistically (Finlayson 1961; Philpott and Smyth 1967; Watts and Aslin 1974; Newsome and Corbett 1975; Carstairs 1976). Unfortunately, detailed information on breeding seasons of desert-dwelling dasyurids is limited. Dasyuroides byrnei, an inhabitant of central Australian gibber plains, is polyoestrous and probably breeds from April to December (Woolley 19710, 1973). Dasycercus cristicauda is found in sandy country in central Australia; it appears to be monoestrous and breeds in May-July, but this information may not be definitive (Woolley 1971a, 1973). Sminthopsis nzacroura from north-western Queensland is polyoestrous, but in the laboratory breeds only in a strictly defined period from July
S. R.Morton
to February (Godfrey 1969b). Antechinomys laniger from south-western Queensland is polyoestrous in the laboratory (Woolley, personal communication); although some litters are born in the wild in November (Woolley 1973), the precise breeding season is unknown. There is no evidence of opportunistic breeding in any of these species, and the timing of breeding appears to be such that young will be weaned in spring or summer. Their reproductive strategies, therefore, may be very similar to that of S. crassicaudata.
The SigniJicance of Caudal Fat Storage In the above discussion, seasonal changes in the caudal fat stores of S. crassicaudata were interpreted as reflecting the immediate energy balance of the animals. Thus, breeding animals store little fat because of the energetic demands of reproduction, and only during autumn, when breeding has ceased and food is still relatively abundant, do the fat reserves increase noticeably (Fig. 8). This interpretation implies that these fat stores are primarily short-term energy reserves, and laboratory study of the size of the reserves supports such a contention. However, some lipid extracted by ether treatment may serve biological functions other than energy storage. Taking the calorific value of fat as 9 . 5 kcal g-I (398 kJ g-I) (Kleiber 1961), Fig. 13 and Table 5 show that the amount of energy stored in the tail [O. 1-0.4 g, or 1-4 kcal(4-2-16.7 kJ)] is small in comparison with that contained in the body t0.8 g, or 7 kcal (29.3 kJ)]. Further, the amount of energy stored as fat (approximately 10 kcal (42 kJ) in total) is small relative to the energy requirements of animals in the laboratory (17 kcal (71 kJ) per day; Morton, unpublished data), and must be an even smaller fraction of the energy requirements of free-living animals. These fat stores, therefore, can provide only limited protection against energy shortage. Nevertheless, their existence shows that there are strong selective forces favouring energy storage, and the selective pressure seems to be short-term variability in insect abundance (Morton 197821). Because the habitat is unprotected from climatic changes, S. crassicaudata probably has to withstand short periods of severe food shortage at irregular intervals. Thus fat storage, together with other energy-conserving devices such as nest-sharing and torpor (Morton 197821, 1978c), provides a partial buffer against unpredictable periods of food shortage. Further insight into the significance of fat storage can be gained by an examination of geographic variation. Populations inhabiting more arid northerly regions may exhibit two distinctive morphological changes-increased tail length and decreased body weight. It is difficult to determine whether the latter trend is universal in S. crassicaudata, since Philpott and Smyth (1967) reported weights of non-breeding animals from south-western Queensland and north-eastern South Australia that were very similar to those of animals from Werribee and Willandra (males, 13.2 g; females, 13.9 g). Because of this uncertainty, discussion will be limited to the significance of variation in tail length. It is clear from Fig. 13 that the longer tails of S. crassicaudata from northern regions contain more fat; the tails of these animals are also capable of becoming more incrassated than the tails of more southerly animals. Selective pressure for greater fat storage probably arose from the less predictable food supply of arid environments. Further, tail length, and presumably the amount of fat storage, are more variable in arid regions than mesic regions. This fact suggests that heterogeneity has arisen in populations inhabiting environments that are more subject
Ecology of Sminthopsis crassicaudata. I11
to random year-to-year fluctuations in food supply. Flux (1971) pointed out that animals do not carry fat unless there is a distinct advantage in doing so, and animals in more constantly favourable environments will divert their energy into other areas. It is conceivable, therefore, that variation in tail length is a result of changing selective pressures for and against fat storage as food abundance varies in different generations. A similar conclusion may apply to variation in nipple number (Table 4). The interpretation of geographic variation in S. crassicaudata advanced above is subject to qualification because of the possibility of thermoregulatory adaptation. Tails may be longer in northern parts of the range of this species that are no more arid than southern areas where the tail is shorter (Morton, unpublished data). Hence, the tail may be shorter in southern S. crassicaudata in accordance with Allen's rule (that appendages become smaller in populations inhabiting colder environments), and selection for fat storage capacity may have been unimportant in determining tail length. Doubt about the causes of geographic variation, however, does not alter the conclusion that variability in food supply is the major selective factor favouring fat storage; such an interpretation is supported by the fact that many other fat-tailed small mammals are desert-dwelling insectivores (Morton, unpublished data).
Evolution of the Life History Polyoestry was interpreted in the above discussion as an evolutionary response to unpredictable short-term variability in food supply. Comparison of the environments of polyoestrous and monoestrous dasyurids supports this conclusion. Many dasyurids from heathland, woodland and forest in southern, eastern and northern Australia are monoestrous, breeding in late winter and spring, e.g. Antechinus stuartii (Woolley 1966; Wood 1970; Lee et al. 1977), A. flavipes (Woolley 1966), A. minimus (Wainer 1976) and A. swainsonii (Lee et al. 1977). One species, however, breeds in autumn (Woolley 1971b). Lee et al. (1977) pointed out that these species live only in environments that receive more than 600 mm of rainfall annually and have relatively predictable seasonal fluctuations in insect numbers. They argue that, although lactation and weaning correspond with the increase in food during spring, birth of a second litter would coincide with the hot, dry summer, and its weaning with declining insect populations in autumn. In view of the prolonged minimum period between birth and weaning in dasyurid marsupials, relative to eutherian mammals of similar size (Woolley 1973; Braithwaite and Lee 1978), these forest-dwelling forms may not have sufficient time to successfully raise a second litter (Lee et al. 1977). However, the time required to raise a litter cannot be the sole determinant of monoestry, since the 120-g Dasyuroides byrnei, a polyoestrous desert-dwelling species, lactates for as much as 4 months (Woolley 1973). Monoestry in forest-dwelling species, therefore, may be due in part to other selective pressures, such as those favouring extended parental care instead of repeated reproduction. Such an interpretation emphasizes that the important factor in the adoption of monoestry or polyoestry by a dasyurid is the relative predictability of the seasonal fluctuation in food supply. Wilbur et al. (1974) pointed out that environmental uncertainty should favour repeated reproduction, so that the reproductive effort of an individual is spread over a greater period of time, and is more likely to correspond with favourable periods. The desert-dwelling dasyurids generally confirm this prediction; possible exceptions, e.g. Dasycercus cristicauda, would repay further investigation.
S. R.Morton
Repeated breeding might also be expected in dasyurids inhabiting environments where the optimal season is both predictable and extended, so as to allow production of more than one litter during the breeding season. Dwyer (1977) observed litters in many months of the year in Antechinus melanurus and A. naso in the New Guinean highlands, and Planigale maculata from subtropical areas of the Northern Territory is polyoestrous in captivity (Aslin 1975). It seems likely that these species have extended or continuous breeding periods, and polyoestry may have evolved in response to lengthy, predictable optimal seasons. It has been suggested that the fluctuating environments of Australian arid regions should favour species that are r-selected (Newsome and Corbett 1975; Richardson 1975; Happold 1976). A comparison of the relevant characteristics of S. crassicaudata with those of the related dasyurid A. stuartii, which inhabits the forests of eastern Australian highlands, shows that certain aspects fit the theoretical correlates of r-selection and K-selection respectively. In A. stuartii intraspecific competition in males is intense, development is slower than in S. crassicaudata (ages at sexual maturity are 11 and 5 months respectively), and both males and females are sedentary (Woolley 1966; Wood 1970; Braithwaite 1974; Lee et al. 1977). In S. crassicaudata intraspecific competition appears to be much less intense, development is the most rapid known in a dasyurid marsupial (see Woolley 1973), and both sexes are highly mobile. However, these are the only correlates that agree with the generally accepted characteristics of r- and K-selection. The litter sizes and life-spans of the two species are similar or identical, and, in direct contrast to the predicted trend, S. crassicaudata is iteroparous whereas male A. stuartii are semelparous (Lee et al. 1977; Braithwaite and Lee 1978). There is evidence, then, that r-selection has played some part in the ecology of S. crassicaudata, but this cannot provide a complete explanation of its life history. The major aim of this study was to determine the primary adaptations enabling S. crassicaudata to exist in open grassland and desert environments (Morton 1978a). Prominent behaviour patterns (winter nest-sharing, high mobility and weak site attachment) appear to be responses to the high variability in food supply (Morton 19783). The reproductive strategy (repeated breeding within an optimal season of uncertain timing) is determined by the relatively unpredictable fluctuations in food supply. The water and energy metabolism of S. crassicaudata show no evidence of specificadaptation to aridity (Morton, unpublished data), and the obvious physiological specializations (torpor and fat storage) seem also to be related to the fluctuating ; study). Thus, the biology of S. crassinature of the environment (Morton 1 9 7 8 ~ this caudata is interpreted as a series of adaptations countering variability in food supply; this variability seems to be the major problem facing a nocturnal insectivore inhabiting open environments, regardless of the aridity of the habitats. Acknowledgments This work forms part of a thesis submitted in partial fulfillment of the requirements for the degree of Ph.D. of the University of Melbourne. I am grateful to Dr A. A. Martin for his supervision and encouragement during this study. I am indebted to the following people for their advice and assistance: Mr R. W. Braithwaite, Dr A. K. Lee, Mr G. D. Parry, Mr B. Miller, Mr and Mrs B. Salau, Mr and Mrs A. L. Morton, and all those who generously assisted with field work. Miss E. Matheson and Mr J. W. Wainer assisted with identification of insects.
Ecology of Sminthopsis crassicaudata. I11
I thank the Melbourne and Metropolitan Board of Works, the Fowlers Gap Management Committee and the National Parks and Wildlife Service of New South Wales for allowing me to work on the Werribee Farm, Fowlers Gap Station and Willandra, respectively. The following persons kindly gave permission to examine specimens in their care: Miss J. M. Dixon (National Museum of Victoria), Mr B. J. Marlow (Australian Museum), Mr P. F. Aitken (South Australian Museum), Dr D. Kitchener (Western Australian Museum), and Dr M. Archer (Queensland Museum). Ms P. Venables helped analyse data and prepared the figures. I am grateful to Ms F. Alexander for her invaluable support and assistance throughout this work and during the preparation of the manuscript. Dr A. A. Martin read and criticized the manuscript. This study was carried out with the support of an Australian Commonwealth Postgraduate Research Award and grants from the M.A. Ingram Trust. References Ahearn, G. A. (1971). Ecological factors affecting population sampling of desert tenebrionid beetles. Am. Midl. Nut. 86, 385-406. Archer, M. (1978). A revision of the dasyurid marsupial genus Sminthopsis Thomas. Bull. Am. Mus. Nut. Hist. (In press.) A s h , H. J. (1975). Reproduction in Antechinus rnaculatus Gould (Dasyuridae). Aust. Wildl. Res. 2, 77-80. Braithwaite, R. W. (1974). Behavioural changes associated with the population cycle of Antechinus stuartii (Marsupialia). Aust. J. Zool. 22, 45-62. Braithwaite, R. W., and Lee, A. K. (1978). A mammalian example of semelparity. Am. Nut. (In press.) Carstairs, J. L. (1976). Population dynamics and movements of Rattus villosissimus (Waite) during the 1966-69 plague at Brunette Downs, N.T. Aust. Wildl. Res. 3, 1-9. Dondale, C. D., Redner, J. H., and Semple, R. B. (1972). Die1 activity periodicities in meadow arthropods. Can. J. Zool. 50, 1155-63. Duffey, E. (1962). A population study of spiders in limestone grassland. Description of study area, sampling methods and population characteristics. J. Anim. Ecol. 31, 571-99. Dwyer, P. D. (1977). Notes on Antechinus and Cevcavtetus (Marsupialia) in theNew Guineahighlands. Pvoc. R. Soc. Queensl. 88, 69-73. Evans, F. C., and Murdoch, W. W. (1968). Taxonomic composition, trophic structure and seasonal occurrence in a grassland insect community. J. Anim. Ecol. 37, 259-73. Ewer, R. F. (1968). A preliminary survey of the behaviour in captivity of the dasyurid marsupial, Srninthopsis crassicaudata (Gould). Z . Tievpsychol. 25, 319-65. Finlayson, H. H. (1933). On mammals from the Lake Eyre basin. Part I. The Dasyuridae. Tvans. R. Soc. S. Aust. 57, 195-202. Finlayson, H. H. (1961). On central Australian mammals. Part IV. The distribution and status of central Australian species. Rec. S. Aust. Mus. 14, 141-91. Flux, J. E. C. (1971). Validity of the kidney fat index for estimating the condition of hares: a discussion. N.Z. J. Sci. 14, 238-44. Godfrey, G. K. (1968). Body-temperatures and torpor in Sminthopsis cvassicaudata and S. larapinta (Marsupialia-Dasyuridae). J. Zool. (Lond.) 156, 499-511. Godfrey, G. K. (1969~). The influence of increased photoperiod on reproduction in the dasyurid marsupial, Sminthopsis crassicaudata. J. Mammal. 50, 132-3. Godfrey, G. K. (19696). Reproduction in a laboratory colony of the marsupial mouse Sminthopsis larapinta (Marsupialia : Dasyuridae). Aust. J. Zool. 17, 637-54. Godfrey, G. K., and Crowcroft, P. (1971). Breeding the fat-tailed marsupial mouse Sminthopsis crassicaudata in captivity. Znt. Zoo Yearb. 11, 33-8. Greenslade, P. J. M. (1964). Pitfall trapping as a method for studying populations of Carabidae (Coleoptera). J. Anirn. Ecol. 33, 301-10.
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Manuscript received 7 November 1977
