Moderate water restriction differentially constrains reproduction in two species of dwarf hamster (Phodopus)

STEPHEN J. SCRIBNER AND KATHERINE E. WYNNE-EDWARDS' Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada

Received November 2, 1993 Accepted July 7, 1994

SCRIBNER, S. J., and WYNNE-EDWARDS, K.E. 1994. Moderate water restriction differentially constrains reproduction in two species of dwarf hamster (Phodopus). Can. J. Zool. 72: 1589-1596.

The dwarf hamsters Phodopus camphelli and P. sungorus are found in semi-arid areas of Siberia and northern Mongolia, but habitat and diet differences suggest species differences in water regulatory efficiency. These differences were investigated by examining the effect of moderate water restriction (50% of ad libitum consumption) on solitary dams and on their reproductive success. In response to water restriction, P. sungorus dams lost less body mass than P. camphelli dams, and despite similar litter sizes, P. sungorus produced heavier litters and pups than P. camphelli, indicating that P. sungorus pups were larger. These results suggest that P. sungorus is more tolerant of water restriction than P. campbelli. In a second experiment the possibility that paternal care may mitigate the effects of water restriction was examined by leaving the mated pair together throughout lactation. Pairing reduced mass loss by P. camphelli dams and increased the proportion of large P. campbelli pups at weaning, but had no effect on these measures in P. sungorus, eliminating interspecific differences in responses to water restriction. Results suggest that biparental care may be a facultative response to environmental stress in P. camphelli.

SCRIBNER, S. J., et WYNNE-EDWARDS, K.E. 1994. Moderate water restriction differentially constrains reproduction in two species of dwarf hamster (Phodopus). Can. J. Zool. 72 : 1589-1596.

Les hamsters nains Phodopus camphelli et P. sungorus vivent dans les rkgions semi-arides de la Sibkrie et du nord de la Mongolie, mais les diffkrences d'habitat et de rkgime alimentaire entre ces espkces permettent de croire que l'efficacitk de leur contr6le hydrique est Cgalement diffkrent. Dans une premikre expkrience, Expkrience I, l'effet d'une restriction mitigke de la consommation d'eau (50% de la consommation ad libitum) sur des femelles solitaires et sur leur succks a la reproduction a kt6 examine. A la suite du traitement, la perte de masse enregistrke chez les femelles de P. sungorus ktait moins importante que celle enregistrke chez les femelles de P. camphelli et, mEme si les portkes Ctaient semblables, les portkes et les petits de P. sungorus ktaient plus lourds que ceux de P. camphelli, ce qui semble indiquer que les petits de P. sungorus sont plus gros. Ces rksultats semblent indiquer que P. sungorus a une tolkrance plus grande a une restriction de la consommation d'eau que P. camphelli. Au cours de 1'Expkrience 11, mile et femelle d'un couple ktaient laissCs ensemble pendant toute la pkriode d'allaitement dans le but d'kprouver I'hypothkse selon laquelle les soins paternels peuvent adoucir les effets de la restriction d'eau. Les femelles des couples de P. camphelli laissks ensemble ont subi une perte de masse moins importante et la proportion de leurs petits de grande taille au moment du sevrage ktait plus ClevCe, variables qui n'ont pas changk chez P. sungorus, ce qui klimine la possibilitk de diffkrences interspkcifiques dans la rkaction 21 une restriction d'eau. Les rksultats indiquent que les soins parentaux par le pkre et la mkre constituent peut-Etre une rkaction facultative a un stress environnemental chez P. camphelli.

[Traduit par la Rkdaction]

Introduction Factors influencing reproductive success have been the

focus of intensive theoretical and empirical research (Clutton-Brock 1988). Experimental studies of rodents in the laboratory have demonstrated that stresses within ranges a species might encounter in nature, such as food and water restriction (Baverstock and Watts 1975; Marstellar and Lynch 1987; Schneider and Wade 1989 ) or low ambient temperature (Marstellar and Lynch 1987; Gubernick et al. 1993), affect reproductive success. Likewise, social factors, including the extent of paternal care (Dudley 1974; Wynne-Edwards and Lisk 1989; Gubernick et al. 1993), may influence reproductive success under particular ecological conditions (Kleiman 1977; Clutton-Brock 1989). Field studies of large diurnal species have supported evolutionary, arguments (Barash 1975; Svendsen 1989; Tabor and Macdonald 1992); however, the nocturnal and fossorial habits of most small rodents have largely precluded direct observations in the wild. Debate about the applicability of laboratory studies has been concerned with physiological acclimatization induced by laboratory rearing (Sahni et al. 1993) and the potential for

I Author to whom all correspondence should be addressed.

the close proximity between individuals to result in artificially high levels of paternal investment in young (Dewsbury 1985; Storey and Snow 1987; Xia and Millar 1988). Nevertheless, field studies have confirmed evidence for paternal care obtained in the laboratory in a number of species (Hofmann et al. 1984; Ribble and Salvioni 1990; Schug et al. 1992).

Dwarf hamsters of the genus Phodopus provide an ideal model to investigate the effects of social and environmental conditions on reproductive success. In the Dungarian hamster, P. campbelli, solitary mothers housed at an ambient temperature of approximately 21 "C reared less than 50% of pups, while the continued presence of the male throughout lactation improved pup survival to over 95% (Wynne- Edwards 1987). In contrast, pup survival at 21°C in the Siberian hamster P. sungorus was high and unaffected by the presence of the male ( Wynne-Edwards and Lisk 1989). Supporting this evidence that paternal presence improves reproductive success in P. campbelli but not in P. sungorus, P. campbelli males spend considerable time alone with the litter, while P. sungorus males are rarely alone with the litter, even in a small laboratory cage (K.E. Wynne-Edwards, submitted for publication). When ambient temperature in the laboratory was reduced to 4OC, reproductive success in

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P.sungorus was unaffected, while pup survival in P. carnpbelli was significantly reduced, and in both species paternal presence was essential for pups to survive ( Wynne-Edwards and Lisk 1989). Responses to other environmental stresses have not yet been compared in these species.

Both P. carnpbelli and P. sungorus are found in the arid continental climate of south-central Siberia and northern Mongolia, but they are not sympatric (Flint 1966). The habitat of P. carnphelli is stabilized sand dunes (Wynne-Edwards et al. 1992), while that of P. sungorus is shortgrass steppe (K.E. Wynne-Edwards, A.V. Surov, and A.Y. Telitzina, unpublished data), with average rainfall during the breeding season (April to September) of 172 + 47 and 3 12 5 57 mm, respectively (weather stations near Erzin, Tuva (50.16"N, 95.14"E), and Abakan, Hakasskaya region (53.43"N, 9 1.26"E, respectively), from 1980 to 1988).

The water-conserving ability of rodents is positively correlated with habitat aridity (Schmidt-Nielson and Schmidt-Nielson 1952) and diet dryness (MacMillen 1983), granivores typically being more efficient water regulators than omnivores (Kam and Degen 1991; Degen and Kam 1992). Phodopus sungorus is primarily granivorous, consuming seeds of at least 5 1 species of plants, only occasionally taking insects (beetles) (Flint 1966). Phodopus carnpbelli is comparatively omnivorous' and commonly supplements its seed diet with insects (K.E. Wynne-Edwards, A.V. Surov, and A.Y. Telitzina, unpublished data), which contain up to 70% water (Kurta et al. 1989). Laboratory studies have reported low water requirements for P. sungorus (Figala et al. 1973; Schierwater and Klingel 1986), whose urine concentration can approach that of true desert rodents when water stressed (Trojan 1977, 1979). The water-conserving ability of P. carnphelli has not been examined.

In arid habitats water stress varies with season and with female reproductive status (Oswald et al. 1993), owing to the additional water demands of lactation (Baverstock and Watts 1975; Konig et al. 1988). This study was designed to compare the effects of moderate water restriction and paternal presence on reproductive success in each species of dwarf hamster. Female condition, pup survival, and pup and litter mass were measured for species and treatment comparisons.

Methods

Animals Dwarf hamsters (P. carnpbelli and P. sungorus) were obtained

from a breeding colony that had most recently been outbred with wild-caught hamsters in 1990. Animals were housed in plastic cages (27 X 2 1 X 14 cm) with wood shavings for bedding and maintained on a 14 h light : 10 h dark illumination cycle (lights off at 15:30). The temperature was maintained at 18 + 1 OC to approximate stable burrow temperatures in the wild (K.E. Wynne-Edwards, A.V. Surov, and A.Y. Telitzina, unpublished data). The estrous cycle of adult females is typically 4 days, with mating occurring during a 4- to 6-h period beginning around lights off (Erb et al. 1993). Gestation and lactation are 18 days each, and because females exhibit a fertile postpartum estrus, simultaneous gestation and lactation are common ( Meyer 1 967 ).

Water availability All hamsters received rodent chow (Purina 5001 ) ad libitum and

a mixed bird seed supplement (2.5 g /d per adult). This food contained approximately 10% free water as determined by oven-drying to constant mass at 70°C. On this diet, water

consumption of nonpregnant, nonlactating female dwarf hamsters was 4 - 6 mL /d ( a maximum, since values include spillage). Trojan ( 1979) reported a mean of 3.29 mL/d (SE = 0.19) for adult P. sungorus on a standard diet of rodent pellets ( 10% free water).

In this study no water bottle was provided, and water intake of hamsters was controlled by providing fresh apple (with seeds and cores removed) as the sole source of free water (approximately 88% of fresh mass determined by oven-drying at 70°C). Apple was chosen because Figala et al. ( 1973 ) had demonstrated that P. sungorus could be reared on a diet of dry food and fresh apple. Pilot studies in this laboratory confirmed that hamsters of either species reared pups of comparable mass when provided with fresh apple ad libitum (20- 25 g /d ) or a water bottle. Leftover apple was removed from the cage each day. Adults showed no external signs of dehydrati~n.~

Rodents from a range of arid to semi-arid habitats tolerate prolonged periods of moderate water restriction and experience only small decreases in body mass (<20%), relying on water obtained from food to help balance their needs (e.g., Willems and Armitage 1975; Dailey and Haines 1981; Edwards et al. 1983). Laboratory-reared P. sungorus maintain 85% of their initial body mass when water is restricted to 50% of ad libitum consumption (Trojan 1979). As water and succulent food is less available in the wild than in the laboratory, a 50% or more reduction of ad libitum water is likely to be a common natural occurrence (Willems and Armitage 1975; Trojan 1979). Hamsters on the water-restricted treatment received 2.0 + 0.1 g/d of fresh apple per adult ( approximately 1.8 mL /d water).

Water consumption of females during lactation is greater than that of nonlactating females (Baverstock and Watts 1975; Konig et al. 1988). Pilot studies in which drinking water was supplied ad libitum indicated that water consumption in dwarf hamsters approximately doubles during midlactation. This study was not designed to examine the effects of severe water restriction on reproduction, therefore water intake of females was maintained at approximately 50% throughout lactation by increasing the portion of fresh apple according to the following schedule: 2.0 g /d on days 0 - 5; 2.5 g /d on days 6 - 8; 3.0g/d on days 9-11; 3.5 g/d on days 12-15; and 4.0 g/d on days 16 - 18. Hamsters on this diet showed only slight dehydration, assessed by dorsal skin resilience, which did not change over the lactation period.

Experiment I : male absent Experimental animals consisted of virgin females aged 60 - 90 d

and males with previous mating experience. These hamsters were assigned at random to either the water ad libitum or water-restriction treatment, which began 4 -7 days prior to pairing. The pair remained together until the day of parturition, when the male was removed from the cage no sooner than 6 h and no later than 18 h after lights off to allow for a postpartum mating and to minimize pregnancy blocking responses (Wynne-Edwards et al. 1987). No attempt was made to record postpartum matings.

Experiment 2: male present The protocol for experiment 1 was followed, but the pair remained

together throughout lactation. On the water-restriction treatment, the portion of apple provided during lactation was increased by 2.0 g /d for the male. No attempt was made to determine which adult actually consumed the apple.

Data collection Beginning 18 d after pairing, cages were checked daily

(approximately 2 h prior to lights off) for the presence of pups. The day that pups were first seen was designated postpartum day 0 (PPD O), and each pup and both parents were individually weighed to the nearest 0.1 g. Pups were sexed (ano-genital distance) and

*Determined according to the resilience of the dorsal skin when gathered, lightly pinched and twisted, and released (Queen's University Animal Care Proposal Approval No. 92-88.)

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SCRIBNER AND WYNNE-EDWARDS 1591

TABLE 1. Responses of solitary dwarf hamster dams and their litters to water availability

Phodopus camphelli Phodopus sungorus Species comparison

Response N PPD 0 PPD 18 N PPD 0 PPD 18 PPD 0 PPD 18

(a) Latency to parturition (d) Water ad libitum Water restricted

(h) Mass of damu (g) Water ad libitum Water restricted

(c) No. of dams with second litter Water ad libitum Water restricted

(d) Litter sizeu (no. of pups) Water ad libitum Water restricted

( e ) Litter mass (g) Water ad libitum Water restricted

( f ) No. of high-quality pups Water ad libitum Water restricted

(g) No. of high-quality litters Water ad libitum Water restricted

NOTE: Values are given as the meap 2 SE. Values significantly different from the value directly above are designated as follows: *, p < 0.05; **, p < 0.01; ***, p < 0.001.

" Values for PPD 18 are the mean change from PPD 0 to PPD 18.

uniquely marked with a felt-tipped pen. The sex of each pup was Results confirmed on PPD 9, with 91% of pups sexed correctly on PPD 0. No attempt was made to standardize litter size, as change in litter size Experiment

was a variable of interest. Data were collected from 10 water ad libitum litters Pups were weighed and identifying marks were refreshed daily ( 5 9 PUPS) and 13 water-restricted litters ( 65 Pups) in

within 2 h of lights off. After PPD 12, when the pups began eating P. camphelli, and from 10 water ad libitum litters ( 56 pups) hard food, their cheek pouches were expressed prior to weighing. On and 9 water-restricted litters ( 44 pups) in P. sungorus. PPD 18, pups were weighed, weaned, and returned to the colony. If a second litter was born on PPD 18, those pups were weighed and sexed. On PPD 18, adults were also reweighed. Dams were killed by cervical dislocation and their reproductive tract was removed and described, and the presence, number, size, and developmental stage of embryos (Edwards et al. 1994) within the uterus were noted.

Eflects of water availability on the dam Water availability had no effect on latency to parturition

(number of days from pairing with the mate to parturition) in P. camphelli, while water restriction almost doubled latency to parturition in P. sungorus (Table l a ; Mann -Whitney, z = 2.8, p = 0.005 ). Phodopus campbelli females gave birth at the expected time (approximately one-half of a 4-day estrous cycle followed by 18 d of gestation) (Erb et al. 1993), while 5 110 water ad libitum and 819 water-restricted P. sungorus females took longer than 22 days to give birth, resulting in species differences (Fisher's exact probability <0.016 for both treatments).

O n PPD 0 there was no interspecific difference in the mass of dams in either water-availability treatment (Table l h ) . Water-restricted females lost mass by PPD 18 ( Wilcoxon, z > 2.6, p < 0.008 for both species), although P. camphelli females lost more mass than P. sungorus females (Mann - Whitney, z = 3.9, p < 0.001 ). No attempt was made to correct for mass of embryos in utero o r pups recently born.

Water restriction similarly affected the probability of pregnancy with a second litter in each species. Pregnancy was confirmed by two or more of ( i ) large, well-vascularized ovarian corpora lutea, ( i i ) recognizable embryos, and ( iii) embryonic heartbeats (Erb and Wynne-Edwards 1993 ). On PPD 18, 9 /10 water ad libitum females of both species were pregnant, but only 2 113 (P. camphelli) and 119 (P. sungorus) water-restricted females were pregnant

Estimates of pup quality Under these husbandry conditions, some very small pups (less than

50% of the mean mass on PPD 18) are alive on PPD 18 that would not be expected to survive under natural conditions. Since the minimum dispersal mass of juvenile P. sungorus in the wild is 12.3 + 0.6 g, in earlier studies a conservative threshold mass of 1 1.5 g was used to quantify the number of pups that had attained dispersal mass by weaning ( Wynne-Edwards 1987; Wynne-Edwards and Lisk 1989). Likewise, in this study, high-quality pups were defined as individuals with mass 2 1 1.5 g on PPD 18. Litter quality was evaluated as the number of litters containing at least one high-quality pup on PPD 18.

Data analysis X' tests and Fisher's exact probabilities were used to analyze pup

survival, pup sex ratio, frequency of lactational pregnancies, and pup and litter quality. There were significant departures from normality in the distributions of most of the continuous dependent variables (Shapiro-Wilk test). Given the small sample sizes, data were not transformed and less powerful nonparametric analyses (Mann- Whitney U test and Wilcoxon's paired sample test) were employed. Analyses did not consider the sex of pups as a variable, as no PPD 0 or PPD 18 data showed any significant difference between sexes. All values are reported as means + SE.

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TABLE 2. Responses of paired dwarf hamster dams and their litters to water availability

Response

Phodopus camphelli Phodopus sungorus Species comparison

N PPD 0 PPD 18 N PPD 0 PPD 18 PPD 0 PPD 18

(a) Latency to parturition (d) Water ad libitum Water restricted

(b) Mass of dam" (g) Water ad libitum Water restricted

(c) No. of dams with second litter Water ad libitum Water restricted

(d) Litter size" (no. of pups) Water ad libitum Water restricted

(e) Litter mass (g) Water ad libitum Water restricted

( f ) No. of high-quality pups Water ad libitum Water restricted

(g) No. of high-quality litters Water ad libitum Water restricted

NOTE: Values are given as the mFan + SE. Values significantly different from the value above are designated as follows: * ,p < 0.05; **, p < 0.01; ***,p < 0.001. " Values for PPD 18 are the mean change from PPD 0 to PPD 18.

(Table lc; Fisher's exact probability < 0.001 for both Quality of pups and litters species). Two water ad libitum P. campbelli dams gave birth On the water ad libitum treatment, 48/54 P. campbelli and on PPD 18, and developmental stages of the remaining 53/54 P. sungorus pups met the criterion of high-quality pups pregnancies were estimated at 6 - 14 d (Edwards et al. 1994). on PPD 18 (Table If ). When water was restricted, only 3/43

Litter size and pup survival through PPD 18 On PPD 0, water availability had no effect on mean litter

size in either species, nor was there an interspecific difference in litter size (Table Id; Mann-Whitney, z < 1.7, p > 0.07 for all comparisons). By PPD 18, water-restricted litters were smaller than water ad libitum litters in P. sungorus only (Mann -Whitney, z = 3.4, p < 0.001 ). Pup killing was never observed, although dead pups were always consumed. Pup losses occurred in 3/10 water ad libitum and 9/13 water- restricted P. campbelli litters and in 1/10 and 10/10 P. sungorus litters. All litters contained at least one surviving pup on PPD 18, and pup survival in water ad libitum litters was greater than in water-restricted litters (Fig. la; x2, > 20, p < 0.001 for both species). There was no interspecific difference in the proportion of pups still alive on PPD 18 (x2, < 1.2, p > 0.27) or in the time course of pup mortality within either treatment (Fig. la). Pup death occurred as late as PPD 9 on the water ad libitum treatment and as late as PPD 15 when water was restricted.

Litter mass Total mass of litters was compared on PPD 0 and PPD 18.

Water ad libitum litters were heavier than water-restricted litters at both ages in both species (Table le; Mann - Whitney, z > 2.8, p < 0.004). No interspecific differences in the mass of water ad libitum litters were found. In the water-restricted treatment P. sungorus litters were as heavy as P. campbelli litters on PPD 0, but were heavier than P. campbelli litters on PPD 18 (Mann -Whitney, z = 2.7, p = 0.008).

P. campbelli pups reached 11.5 g, while 19/44 P. sungorus pups did, resulting in a species difference (x2, = 15, p < 0.001). In both species, all litters contained at least one high-quality pup on the water ad libitum treatment, but more P. sungorus litters contained high-quality pups than P. campbelli litters when water was restricted (Table lg; Fisher's exact probability = 0.006).

Experiment 2: male present Data were collected from 10 water ad libitum litters

(64 pups) and 18 water-restricted litters (85 pups) in P. campbelli and from 10 water ad libitum litters (55 pups) and 9 water-restricted litters (50 pups) in P. sungorus.

Effects of water availability on the adults Latency to parturition was longer than 22 d in 6/18

P. campbelli and 819 P. sungorus water-restricted pairs, resulting in a species difference (Table 2a; Mann -Whitney, z = 2.8, p = 0.005). Water-restricted dams lost more mass than water ad libitum dams in both species (Table 2b; Mann -Whitney, z > 3.0, p < 0.003). Relative to solitary dams, pairing significantly reduced mass lost by water- restricted P. campbelli dams (Mann -Whitney, z = 3.7, p < 0.001), but had no effect in P. sungorus dams, so the interspecific difference (Table lb ) was eliminated. As in experiment 1, dam mass was not corrected for embryo or pup contributions. Water availability had no effect on change in body mass of P. campbelli males (water ad libitum, + 0.4 +_

0.5 g; water restricted, -0.4 + 0.6 g; Mann -Whitney, z = 0.7, p = 0.5 ), while P. sungorus males receiving water and ad libitum gained an average of 2.7 ? 0.6 g and

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SCRIBNER AND WYNNE-EDWARDS

Day of lactation

FIG. 1. Proportion of dwarf hamster pups born that were still alive on each day of lactation in experiment 1 when the dam was alone ( a ) and in experiment 2 when the male parent was also present ( h ) . All litters contained at least one surviving pup on PPD 18. Sample sizes are given in the text. A, P. camphelli, water ad libitum; 0, P. sungorus, water ad libitum; a, P. camphelli, water restricted; 0, P. sungorus, water restricted.

water-restricted males lost an average of 1.1 -+ 0.6 g (Mann -Whitney, z = 3.4, p < 0.00 1 ).

Pairing did not significanily change the proportion of females pregnant with a second litter in either species or treatment (Table 2c). One P. campbelli dam gave birth on PPD 18. Age of embryonic litters of water ad libitum females was not significantly affected by pairing. Sample sizes for water-restricted females were too small to allow species differences to be detected,

Litter size and pup survival through PPD 18 On PPD 0, water-restricted P. campbelli litters were smaller

than water ad libitum litters (Mann-Whitney, z = 2.7, p = 0.008), but neither differed in size from P. sungorus litters (Table 2d). By PPD 18, the decrease in size of water-restricted litters was greater than that of water ad libitum litters for P. campbelli (Mann-Whitney, z = 2.6, p = 0.008), but not for P. sungorus. Paternal presence did not significantly affect litter size at PPD 18 for either species or either water-availability treatment.

Pup losses occurred in 1/10 water ad libitum and 11/18 water-restricted P. campbelli litters and in 2/10 and 619 P. sungorus litters. No species difference in the proportion of pups still alive on PPDl8 within either water-availability treatment was found (x2, < 2.4, p 1 0.12). The time course of pup mortality during lactation followed a similar pattern in each species (Fig. 16). Pup loss occurred as late as PPD 3 on the water ad libitum treatment and as late as PPD 12 when water was restricted.

Litter mass As in experiment 1, water ad libitum litters of both species

were heavier than water-restricted litters at both ages (Table 2e; Mann-Whitney, z > 2.7, p < 0.006 for all analyses). There was no interspecific difference in mass of water ad libitum litters at either age, but water-restricted P. sungorus litters were heavier than P. campbelli litters at both ages (Mann- Whitney, z > 2.3, p < 0.022 for both ages). Pairing increased litter mass on PPD 18 in water-restricted P. sungorus litters (Mann-Whitney, z = 2.9, p = 0.005) but not in P. campbelli litters.

Quality of pups and litters Water restriction decreased the number of pups reaching

threshold mass (x2, > 53, p < 0.001 for both species), but there was no species difference (Table 2f). Pairing did not significantly improve the proportion of water ad libitum or water-restricted pups reaching threshold mass in either species. Pairing, however, did eliminate interspecific differences in the proportions of water-restricted pups reaching threshold mass (Table If), as more high-quality P. campbelli pups and fewer high-quality P. sungorus pups were raised.

All water ad libitum litters of both species contained at least one pup above threshold mass on PPD 18 (Table 2g). Water restriction reduced the number of litters with at least one pup above threshold mass in both species (Fisher's exact probability < 0.033 ), and there was no interspecific difference in this effect. Pairing did not affect the proportion of water-restricted litters with at least one pup above the threshold mass on PPD 18; however, sample sizes were small.

Discussion While it was predicted on the basis of diet differences that

granivorous P. sungorus would require less free water than omnivorus P. campbelli, average rainfall during the breeding season suggested the opposite pattern of adaptation in each of the two species. Responses to water restriction clearly suggest that P. sungorus is less stressed by water restriction during reproduction than P. campbelli. Of seven measures of effects of water restriction on the condition and reproductive success of solitary females, four indicate that P. sungorus tolerated water restriction better than P. campbelli. When water restricted, P. campbelli females lost more mass during reproduction, and reared litters and pups of less mass at PPD 18 than P. sungorus females. Of the three remaining measures of effects of water restriction, there was no difference in the litter size or number of females with a concurrent pregnancy at PPD 18, while P. campbelli females exhibited shorter latency to parturition. When the same criteria were applied to paired females, paternal presence

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eliminated the species difference in the effect of water restriction in all but one test (litter mass), suggesting that the presence of both parents was able to compensate for water restriction in P. camphelli, while having limited, if any, effect in P. sungorus.

Decreased reproductive success in response to water restriction may be attributable to inadequate milk quantity. Pup cannibalism increases as food is restricted and ambient temperature decreases in Mus musculus (Marstellar and Lynch 1987) and Mesocricetus auratus (Schneider and Wade 1989), improving the efficiency of lactation (Konig et al. 1988). As lactation proceeds, dams increase their water consumption to meet the demands of growing pups (Konig et al. 1988), although this effect is smaller in desert rodents (Baverstock and Watts 1975). In this study the apple ration was increased during lactation to meet this demand in Phodopus spp., but may not have eliminated the increasing water stress. Pup mortality in the water-restricted groups persisted through the first half of lactation and may reflect an attempt to match litter size with lactational resources.

Lower reproductive success of water-restricted females may be due to inadequate maternal care, through the indirect effect of restriction on maternal thermoregulation. Rattus lutreolus can dissipate 100% of its total heat through evaporative water loss (Collins 1973), which is an important avenue of heat dissipation during gestation (Wilson and Stricker 1979) and lactation (Knecht et al. 1980). In non- lactating rats, dehydration substantially impairs evaporative cooling (Stricker and Hainsworth 1970). Rodents from arid and semi-arid habitats reduce evaporative water loss as an adaptation for water conservation (Du Plessis et al. 1989). Respiratory water loss in adult male and nonlactating female P. sungorus accounts for 20% of total heat loss at 1g0C, and increases to only 40% at a maximum ambient temperature of 34°C (at which point the animals also use postural changes and saliva spreading to thermoregulate) (Heldmaier 1975). During lactation, the elevated body temperature of dwarf hamster (Scribner and Wynne-Edwards 1994a) and rat (Jans and Leon 1983) dams increases further while they are in contact with pups, and they temporarily abandon the litter to dissipate the heat load (Leon et al. 1978; Jans and Leon 1983; Scribner and Wynne- Edwards 1994b). Since water restriction reduces the water available for evaporative cooling, and hence heat dissipation cooling of lactating females, behavioural heat loss may increase and less time may be spent with the litter, retarding pup growth.

Uniformly high pup survival of solitary, water ad libitum females contrasts with previous findings in which solitary P. campbelli females, but not P. sungorus females, experienced reduced pup survival ( Wynne-Edwards and Lisk 1989). One experimental difference was the ambient temperature in each study ( 1 8 vs. 2 1 "C). Small differences in ambient temperature affect maternal care in Peromyscus californicus (Gubernick et al. 1993), Gerhillus pusillus (Buffenstein 1985), and rats (Leon et al. 1978), and may also affect maternal care in Phodopus spp. (Scribner and Wynne-Edwards 1994 b ). The higher ambient temperature in previous studies (Wynne-Edwards and Lisk 1989) may have impaired maternal behaviour more than the current tem- perature, 18"C, which matches measured burrow temperatures in the wild (K.E. Wynne-Edwards, A.V. Surov, and A.Y. Telitzina, unpublished data). Therefore, both elevated ambient temperature

and water restriction may affect reproductive success by compromising maternal heat dissipation.

Wynne-Edwards and Lisk ( 1989) also reported that pairing improved reproductive success in P. campbelli but not in P. sungorus. In this study pairing also improved reproductive success and eliminated interspecific differences in maternal mass and pup quality in the water-restricted treatment. Unambiguous interpretation of these results is complicated by the extra 2.0 g of apple available in cages with the two adults, since the apple could have been eaten by either adult (or the older pups). This study could not distinguish between the benefit of paternal presence in P. campbelli as a result of paternal care and the benefit gained as a result of the dam consuming some of the apple supplied for the male. However, in P. sungorus, water-restricted males lost mass and water ad libitum males gained mass, while the mass of P. campbelli males was unaffected by water treatment. Under laboratory conditions, P. sungorus females are sometimes dominant over males, while P. campbelli females are always subordinate to males ( Wynne-Edwards and Lisk 1987). The loss of mass of water-restricted P. sungorus males suggests that they may have acquired less of the 2.0 g of apple.

Thus, the evidence from intersexual dominance (Wynne- Edwards and Lisk 1987) and male mass change suggests that P. campbelli dams and pups did not benefit from paternal presence through increased access to water. K.E. Wynne- Edwards (submitted for publication) recently found that male P. campbelli are alone on the nest when the dam is absent, which results in a decrease of about 50% in the time that litters are left alone. As pup growth requires exogenous heat, P. campbelli males may play a critical role in warming the pups during the dam's absence, as has been suggested in Peromyscus californicus (Dudley 1974 ; Gubernick and Alberts 1987). Whether paternal behaviour also results in elevated body temperature and disrupted daily behavioural rhythms (Scribner and Wynne-Edwards 1994a) is unknown.

Under optimal conditions, female dwarf hamsters of both species mate on the day of birth of the first litter, and give birth to the second litter 18 days later, by which time the first litter must be ready to disperse (Meyer 1967). Under harsh conditions, lactation may be prolonged to ensure that small pups achieve the threshold mass for successful dispersal. Extension of lactation has been noted in larger mammals in response to natural stresses (e.g., Lee et al. 199 1 ) and could allow sucklings to reach a viable dispersal mass. Present data suggest that delay of the second litter facilitates prolonged lactation. As males in experiment 1 were removed immediately after a ( possible ) postpartum estrus, viable embryos with less than 18 days of development on PPD 18 must have been delayed and not the product of a later mating (in contrast to Parkening and Collins 1991 ). Delayed implantation is common among small rodents (Norris and Adams 197 1; Elwood and Broom 1978; Myers and Master 1983) and would be adaptive in Phodopus spp. when population densities are low and mating opportunities may be rare ( Wynne-Edwards et al. 1992).

Facultative biparental care in P. campbelli may be able to compensate for moderate environmental stress and enhance reproductive success. That P. sungorus is less affected by water restriction and does not gain from paternal presence suggests that this species can physiologically compensate for water and thermoregulatory stresses without impairing reproductive success.

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