Stress and nutrition in the wild.

Abstract

11 Stress and nutrition in the wild M.P. Moshkin1, L.A. Gerlinskaya1, E.L. Zavjalov1, I.E. Kolosova1, K.A. Rogovin2 and J.A. Randall3 1 Institute of Systematics and Ecology of Animals, Siberian Branch of RAS, 630091 Novosibirsk, Frunze str. 11, Russia 2A.N. Severtzov Institute of Ecology and Evolution RAS, 119071 Moscow, Leninskii prospect 33, Russia 3San Francisco State University, San Francisco, USA mmp@eco.nsc.ru Summary Regular monitoring during an 18 year period of the demography and endocrine function of a West Siberian population of water voles (Arvicola terrestris) revealed a close correlation between population density and variation in a stress index that was calculated by principal component analysis from plasma or blood concentrations of corticosterone, progesterone, testosterone, estradiol, and free fatty acids (FFA). Maximum stress a s indicated by maximum hypothalamicpituitaryadrenal (HPA) activity was not coincident with peak population density but was delayed by two years. This was accompanied by, typical for starvation, a decrease in body mass and an increase in FFA. Analysis of food conditions revealed food shortages in the winter and decreasing food quality (digestibility) in the summer during periods of maximum stress. Besides food shortage, an additional stress factor during the decline phase of water vole population cycles is the change of food plant distribution from even to patchy. Concentration of animals on the small patches stimulates intermale competition, which induced hypersecretion of stress hormones. In another study, great gerbils (Rhombomys opimus ) that inhabit Asian temperate deserts sequentially consume a number of food plants during the year. Measurements of faecal corticosterone in adult males revealed a negative correlation between HPA activity in the spring and abundance of succulents in the summer. Although succulents seem to be a minor component of the spring diet, it appeared that in the home range a low production of new sprouts by these plants because of adverse growing conditions area resulted in HPA activation and increased mortality of adult males. In turn, the high mortality rate of adults probably allows the younger part of the population to overcome food shortage in dry summers. Keywords: wild rodents, stress, nutrition, endocrine function, maturation, pregnancy, survival Introduction Christian (1950, 1961, 1963, 1971) proposed that physiological consequences of stress are central to the densitydependent control of population demography. S t ress induced by social factors may suppress reproduction and increase mortality rate in mammalian populations. Due to this very popular hypothesis, the relationship between social environment and function of stressrelated systems has been emphasized in most research of populations of wild mammals (Shilov 1967; Andrews 1979; Bradley et al. 1980; Lee and McDonald 1985; Sapolsky 1990; Boonstra and Boag 1992; Creel et al. 1996; Novikov and Moshkin 1999). Little or no attention has been paid to effects of nonsocial stressors such as malnutrition, and other factors. However, both short and longterm food limitation induces typical stress responses detected by activation of hypothalamic pituitaryadrenal (HPA) and sympathoadrenal systems (Rossi et al. 1980; Jacobson et al. 1997; Mercer et al. 1997; Giovambattista et al. 2000). Hormones and neurotransmitters of these systems play key roles in mobilization of the energy reserves that are stored in liver and in fat tissue (Panin 1978). Additionally, glucocorticoids, in conjunction with cytokines, suppress thyroidal activity and reduce basal metabolic rate (Ingenbleek and Bernstein 1999). Also, corticosteroids stimulate synthesis and secretion of hypothalamic neuropeptide Y, which inhibits food intake (Strack et al. 1995). Both resource mobilizing and energy saving effects of stress hormones help animals to survive during food shortages. Here, we demonstrate three different ways of foodrelated modulation of HPA activity in wild populations of water voles, Arvicola terrestris, and great gerbils, Rhombomys opimus. First, we discuss the periodic food shortage in the population cycles of the water vole; second, we examine results of the spatial distribution of the food plants that shapes spatial structure in a local population of herbivores (water vole as an example); and third, we show the possible stress modulated effect of the minor compounds of plant sprouts, the abundance of which correlates negatively with HPA activity. Recent Advances in Animal Nutrition in Australia, Volume 14 (2003) 12 Moshkin et al. Stress and food conditions in population cycle of water vole Dynamics of stress index Water voles are semiaquatic rodents that occupy banks of small streams and marshes during the breeding season and move to meadows and agricultural fields at the fall. The seasonal exodus from breeding area to wintering area generates serious danger for domestic crops and young forests. Also, water voles take part in circulation of some infections such as rabbitfever. Both agricultural and epidemic problems have drawn attention of scientists to water vole cycles in West Siberia (Panteleev 1968; Maksimov 1977). Our study of a water vole population was carried out in a subtaiga region of the Baraba lowland, in the vicinity of Lisii Norki, Novosibirsk region, West Siberia (55�50N, 80�00E). During 19801997, we captured water voles every year from May to September using Kulunda livetraps. Blood samples were collected for endocrine study from animals that were kept in individual cages during 27 days after trapping. Details of methods of collection and analysis of blood samples are described in our previous papers (Moshkin 1989; Gerlinskaya et al. 1994; Evsikov et al. 1999a). Like other authors (Panteleev 1968; Maksimov 1977) we have found regular fluctuations of population size in water voles with an interval of about 68 years between the peaks (Figure 1). The numbers increase following heightening water levels in swamps and streams. Water voles show changes from year to year in levels of circulating free fatty acids (FFA), glucose, corticosterone, progesterone, testosterone (in males), and estradiol (in females). A principal components calculation (Kendall and Stuart 1966) of annual means of the blood indices revealed that the first component accounted for 40.4 % of all variance in overwintered males and 56.4 % in overwintered females. Annual means of corticosterone, progesterone, and F FA correlated positively, and means of the gonadal hormones correlated negatively with the first principal component (Evsikov et al. 1999a). Correlations between blood glucose and the first principal component were close to zero in both males and females. Since activation of the adrenal cortex and fat releasing mechanisms as well as suppression of the gonadal endocrine function are the typical physiological manifestations of the non specific adaptive syndrome, the first component may be treated as an integrated stress index in water voles. Fluctuations of this stress index from year to year were synchronous with dynamics of population density (Figure 1) but, contrary to Christians prediction of maximum stress at the highest population density (Christian 1950, 1961, 1971), maximum stress followed the peaks of water vole numbers with a two year lag. Maximal manifestation of stress in the decline phase testified to factors other than social pressures as a primary stressor. Figure 1 Dynamics of the population density and stress indexes (first principal component) in overwintered males and females of the water vole. The stress index, expressed in notional units, was derived from principal component analysis of the annual mean values for plasma corticosterone, plasma progesterone, plasma testosterone (in males) or estradiol (in females), blood free fatty acids (FFA), and blood glucose (Evsikov and Moshkin 1994). Analysis of cross_correlations revealed statistically significant relationships between multiannual variations of population density and stress indexes with a 2 year lag (r = 0.71, P<0.01 for males; and r = 0.66, P<0.05 for females). Population density, animals/square km Stress index, conventional units Stress and nutrition in the wild 13 Stress factors in population cycle of water vole In West Siberia the variation from year to year in numbers of water voles is associated with climatic cycles (Maksimov 1977). The increases in population size coincide, as a rule, with the phases of an increase in swamp water impounding that extends areas which water voles can occupy in the breeding season (summer). At the same time, during the autumn exodus to meadows, water voles encounter territorial and food problems because winter habitat (meadows) shrinks with the rising water table. In the phase of peak numbers, water voles almost completely devour the subterranean parts of plants in their wintering sites. As usual, overgrazing of food plants in the peak densities of herbivorous mammals is attenuated due to predators or self regulation to limit population growth (Christian 1961, 1963; Boonstra 1994; Hansson, 1999; Klemola et al. 2000), but water voles are an exception to the density dependent control of reproduction because they are using different feed resources during the summer breeding season and the winter nonbreeding season. In addition, subterranean life in winter presumably protects water voles from the pressures by the many predator species. Due to food shortage after peak winter populations, water voles that successfully overwintered are forced to eat dry grass and bark during several weeks before the spring growth of vegetation whereas the food available for animals that have overwintered during the period of low population density is more digestible fresh grass (Evsikov and Ovchinnikova 1999; Ovchinnikova 2000). Furthermore, population decline generally coincides with a decrease in swamp water impounding. Changing of water levels in swamps and streams is followed by variations in the digestibility of water plants which becomes higher in the phase of population decline and decreases in peak phases (Evsikov and Ovchinnikova 1999). Fall in digestibility coincides with a decrease in body mass and an increase in blood FFA as an indicator of physiological responses to starvation. These factors, therefore, seem to be the main reasons for stress in water voles during population cycles (Figure 2). Demographic consequences of stress At the decline phase of water vole population cycles, newborn males become mature only in the next year after birth. Among the many endocrine mechanisms causing a delayed puberty in males, of special interest is the inhibiting effect of high blood progesterone which during stress has mainly adrenocortical origin (Christian 1971; Bazhan 1991). Acting through the hypothalamic receptors of negative feedback, the progesterone inhibits pituitary gonadotrophin secretion and thereby lowers the rate of sexual maturation of young animals (Collu et al. 1979; FernandezCeladilla et al. 1986). Reciprocal relationship between monthly average concentrations of the blood progesterone and monthly averages of testicular mass in young water vole males (r = 0.71; df = 10; P<0.01) supports the hypothesis that high levels of progesterone can suppress maturation rates through hypothalamic negative feedback (Moshkin 1989). Besides the changes from year to year in maturation rates, variations in the rate of reproduction in water vole population cycles are determined also by embryo mortality that increases during the population decline phase (Evsikov et al. 1999b). Embryo mortality is associated with an increase in blood FFA and a decrease Body mass, g Digestibility, % Figure 2 Dynamics of the body mass, blood concentration of FFA, and food digestibility in overwintered water voles. Values are annual means of males and females � SEM. (Moshkin 1989; Evsikov et al. 1999a; Evsikov and Ovchinnikova 1999). FFA, micromol/l 14 Moshkin et al. in b lood glucose in pregnant f emales (Figure 3). Hypoglycaemia, as well as mobilizing of fat, shows that failure of pregnancy was probably induced by malnutrition. Females with successful pregnancies in the population decline years had higher levels of plasma corticosterone and progesterone than females that failed to maintain pregnancy. A high level of corticosterone in females with successful pregnancy seems contrary to common view that stress leads to an increase in both HPA activity and embryo resorption rate (Ostro et al. 1996; Arck et al . 1997), but it was found that experimental manipulations with level of glucocorticoids in maternal circulation did not influence the frequency of abortions (Sahu and Dominic 1981; de Catanzaro et al . 1991). Moreover maternal requirements for progesterone and glucocorticoids increase considerably during pregnancy under malnutrition, s ince both hormones cooperatively mobilize internal resources to support pregnancy in starved females (Morishige and Leathem 1973; White et al. 1980; Khurana and Paul 1983). Hence, successful pregnancy, especially during the population decline phase, depends on the ability of pregnant females to intensify production of both glucocorticoids and progesterone. Thus, on the one hand, stress inhibits the maturation rate and r educes reproduction in t he decline phase of population cycles but, on the other hand, stress hormones allow successful gestation in some individuals of the water vole population that are experiencing food shortage. Spatial distribution of the food resources and stress Although maximum manifestation of stress did not occur when water vole densities were at a peak, we cannot exclude the stressful effect of social factors. Experimental crowding of the captured water voles revealed activation of the HPA axis in response to inter male aggression (Moshkin 1989; Moshkin et al. 1994). Modern approaches to the assessment of corticosterone in faeces allow us to study the manifestation of stress in wild animals with minimal disturbance from researchers. Based on these methods, we demonstrated that changes in food from an even to patchy distribution resulted in an increased density of local groups of animals and intermale competition, which induced HPA activity. Spatial distribution and stress were studied in a local settlement of water voles that occupied the bank of irrigation channels in the vicinity of Lisii Norki. The group range (450 m) was bordered by shallow places on both flanks of the deep part of the water channel. We trapped for approximately two weeks during the breeding season in May 2000 and 2001. After these sessions, we captured water voles and kept them for one week in individual cages in natural photoperiod and with food and water ad libitum. Livetraps were set every 10 m on the channel shoreline, and they were checked each night at 4 h intervals. Since the faecal steroids have at least a 34 h lag in response to the changes of hormonal secretion (Gerlinskaya et al. 1993; Harper and Austad 2000), we consider the Figure 3 Plasma corticosterone, plasma progesterone, blood FFA, and blood glucose in pregnant females with normal pregnancy and with embryo resorption. These comparisons have been done only for endocrine data collected in the decline phases of the water vole population cycles. Values are means � SEM. (Moshkin 1989; Evsikov et al. 1999a). * P<0.05, ** P<0.01, *** P<0.001, in comparison with normal pregnancy (Student's t_test). Stress and nutrition in the wild 15 corticosterone and testosterone levels in the faecal samples to reflect a normal, pretrapping, endocrine status of animals. Capture, mark and release (CMR) methods were used. Animals that were trapped more than once were classified as residents in contrast to non residents that were trapped singly. Maximal distance between trapping points was considered a home range of residents. The concentrations of corticosterone in dry faeces were measured by radioimmunoassay using Sigma antibodies (rabbit anticorticosterone) and labelled [1,2,6,7H3] corticosterone (Amersham, UK). Steroids were extracted from faecal samples using procedures described earlier (Gerlinskaya et al. 1993; Rogovin et al. 2003). Forty mg dry faeces were homogenized with distilled water (2 ml) in a glass grinder and centrifuged (15 min; 2000 g). Supernatant was extracted with 3 ml ethyl ether; 2 ml extract was removed, transferred to a new tube, vacuum dried at 37�C, and 300 m l phosphate buffer (pH 7.0) was added. The concentration of corticosterone was measured in the manner specified by Sigma. For assessment of humoral immune response, trapped males were injected intraperitoneally with 0.5 ml of a 2 % suspension (2x108 cells) of sheep red blood cells (SRBC). Six days after injection, we extracted 0.1 ml of blood from the suborbital plexus. SRBC antibody titre was measured using haemoagglutination assay in 96well microplates (Hay and Hudson 1989). Antibody titres were expressed as the log2 of the reciprocal of the highest dilution of plasma showing positive haemoagglutination (Lochmiller et al. 1993). Approximately the same numbers of water voles were captured in 2000 (34 animals) and 2001 (39 animals) in the traps that were set uniformly along the water channel shorelines. In spring 2000, the spatial distribution of captures did not differ from equal success per trap (Figure 4; 2 = 13.0, df = 8, P>0.05), but in spring 2001 when water channels became shallow the abundance of food plants declined in the central part of the trapped area; because water voles were associated with available plants, they occupied flanks of the area and the distribution of captures was clumped (2 = 55.7, df = 8, P<0.001 in comparison with equal distribution). Due to the concentration of water voles in optimal places, the home ranges of resident males were used also by a greater average number of neighbour and non resident males in 2001 (4.83 � 0.94 voles; n = 12) in comparison with 2000 (1.92 � 0.34 voles; n = 12; P = 0.034, MannWhitney test). As a result, the number of skin wounds indicated that intermale aggression was higher in 2001 than in 2000 (Figure 5). Concentration of corticosterone in faeces collected from resident males also increased in 2001 compared with 2000. Since, there were no betweenyear differences in body mass, we can conclude that social pressure rather than malnutrition induced HPA activity in resident males. Stress triggered by intermale competition was accompanied by a reduction in the humoral immune response to SRBC. Spring stress predicts malnutrition in summer Great gerbil and its food The great gerbil, Rhombomys opimus, represents the most socially developed species among rodents in the subfamily Gerbillinae (Muridae, Rodentia) (Naumov and Lobachev 1975; Goltzman et al. 1977; Pavlinov et al. 1990; Gromov 2000). This desert, diurnal and mostly folivorous gerbil (150220 g) lives in compact Figure 4 Distribution of the water vole captures along the bank of an irrigation channel during two_weeks trap sessions in 2000 and in 2001. 16 Moshkin et al. family groups in complex burrows (colonies in Russian zoological literature). Each family group uses one complex burrow (colony) that consists of a system of interconnected underground holes and chambers and a number of isolated holes connected by aboveground paths. A breeding group usually consists of an adult male, one to seven adult females, several juveniles and subadults of previous litters (Kutcheruk et al. 1972; Naumov et al., 1972, Randall et al. 2000; Rogovin et al. in press). We studied the relationships between food plants and HPA activity in adult males of the great gerbil in 1999 and 2000 at the bioreserve Ecocentre Dzeirsan (30o3539o40 N, 64o3164o43O) in Uzbekistan 30 km to the south from Bukhara . Great gerbils sequentially consume a number of food plants during the year (Kutcheruk et al. 1972; Burdelov et al. 1974; Mokrousov 1978). At the site of our research in the early spring (MarchApril) they eat ephemeral annuals (genera Ceratocephala, Hypecoum, Tetracme, Rhoemeria, Papaver, Eremopyrum, Bromus, Scorzonera), followed by perennial shrubs in the late spring (AprilMay) ( Astragalus velosissimus, Ammothamnus leihmannii). Settlements of the great gerbils are associated with the borders of saline depressions with plant communities dominated by annual and perennial succulents of the family Chenopodiaceae (Climacoptera, Salsola, Suaeda). These succulents provide an important source of food during the period of summer and fall drought from late May to November. The haloxylon tree (Haloxilon aphyllum) provides food for the gerbils all the year round, but mostly in the late fall and winter because it is less preferred than ephemeral plants and small succulents. Sampling and assessment We marked and observed gerbils in 1999 from March 29 to May 16 and from October 13 to November 1, and in 2000 from March 31 to May 15 and between October 15 and November 2. We trapped gerbils in wire mesh livetraps (30 x 15 x 15 cm) baited with a mixture of rolled oats, sunflower seeds, carrots, greens, and peanut butter. We marked adults and pups in each family group with numbered ear tags and clipped the light brown guard hairs on the backs and sides of gerbils to expose dark patterns in t he underhairs for individual identification at a distance. We observed gerbils in their respective family groups from a distance of approximately 40 m with binoculars to estimate the total group size, group composition and range of adult and juvenile activity. Continuous observations of family groups helped us to determine dates of pup emergence and their number before marking. All gerbil colonies, including occupied and unoccupied burrow systems in a current season, were mapped at a scale of 1:2000 within an area of 45 ha in 1999, which we extended up to 52 ha in 2000. We mapped the area with a compass, tapeline and an unpublished map of vegetation of the Bioreserve made in 1980 by G.I. Shengbrot. In spring 2001, we corrected the map of distribution of gerbil colonies with a GPS system (GARMIN12). Observational data showed that at least 90% of rodent activity was limited by areas with burrow entrances. We designated these as colony areas and calculated the areas as the territories for family groups. We also estimated distances between colony centres and size of each colony, as defined by the area of burrows in use by a family group in a current season, from maps using convex polygons. We counted abundance and diversity of food plants in the burrow area each family group can use in different seasons: (1) ephemeral grasses (spring food); (2) perennial shrubs (food in late spring and early summer); (3) succulents (summer and fall food); and (4) Haloxylon aphyllum (summer, fall and winter food). We counted the number of ephemeral plants inside a 25 cm2 frame after three random throws of the frame in Figure 5 Skin wounds, body mass, faecal corticosterone, and antibody titre in overwintered water vole. Values are means � SEM. * P<0.05, ** P<0.01, *** P<0.001, in comparison 2000 vs 2001 (Mann_Whitney rank test) Stress and nutrition in the wild 17 the central part of a colony and three throws on the periphery of the same colony. Abundance of ephemeral herbage was expressed as an average number of plants per m2. The number of perennial shrubs and large annual succulents was calculated at four points within 5 m radius colony areas. Two points were randomly selected in the centre and two on the periphery of a colony; height and diameter were measured in 30 examples of each shrub and succulent species and crown volumes (m3) were estimated for assessment of the average abundance of the perennial shrubs and succulents in the 10 m diameter areas. The total number of Haloxylon trees and their crown volumes (m3) were estimated within the colony area and then attributed to the area unit of 5 m radius. We measured succulents in the fall; measurements of all other plants were made at the period of vegetation maximum in the spring. In the spring we collected faeces of the adult male in each family group from the soil surface under livetraps within approximately two hours of capture. We checked traps repeatedly in the morning so that most samples were taken within the first hour after capture. The radioimmunoassay method that was used for assessment of the faecal corticosterone is described above and in Rogovin et al. (2003). This method was elaborated for measurement of faecal corticosterone in herbivorous rodents and it was verified in studies on the water vole, Arvicola terrestris, and the bank vole, Clethrionomys glareolus, and gerbil species. Good correlations between concentrations of corticosterone in blood plasma and faeces collected before and after stress stimuli were found (Gerlinskaya et al. 1993; Moshkin et al. 2001; Gerlinskaya and Zavjalov, pers. comm.). Food plants and spring stress in adult males Spearman rank correlations were calculated between abundance of food plants and physiological status of the adult males trapped in the spring (Table 1). It was quite predictable that body mass of adult males in the spring correlated positively with abundance of the ephemeral grasses, the main food in the spring. Current availability of food (ephemeral grass and perennial shrubs) did not influence HPA activity. At the same time, the abundance of succulents, which great gerbils eat in the late spring and summer, showed a statistically significant negative relationship with concentrations of corticosterone in faeces collected from April 1 to May 7 (Table 1). Two hypotheses might provide an explanation for this unusual relationship between stress in the spring and availability of food in the summer. One hypothesis is that a large population of great gerbils has two effects that induce stress in adult males, namely social pressure, and a decrease in abundance of food plants due to the number of consumers. These two effects could generate a negative relationship between faecal corticosterone and abundance of succulents. Abundance, however, was not significantly related to the number of gerbils counted in each family group in late spring (Table 1) though the partial correlation coefficient between corticosterone concentration and succulent abundance, calculated with controlled group size, was significant (r = 0.327; P<0.05). The second hypothesis is concerned with endocrinological effects of a minor food component. The bestknown example is the influence of plant sprouts on reproductive function in wild rodents (Berger et al. 1981), and the meristematic tissue of young growing grasses contains 6methoxy2 benzoxazolinone (6MBOA) which stimulates maturation in seasonally breeding voles (Nelson 1991; Meek et al. 1995). There are some reports on stress modulated effects of plant compounds. For example, chronic administration of a Gingko biloba extract (Egb 761) reduced basal level of plasma glucocorticoids and inhibited stressinduced corticosterone hypersecretion through a reduction in the number of adrenal benzodiazepine receptors (Amri et al. 1996; Marcilhac et al. 1998). The reduction of HPA response to stress stimuli and sensitization of the hypothalamic negative feedback receptors have been described in experiments on mice and rats that were pretreated by extracts from such plants as Korean or Chinese ginseng, Scutellaria baicalensis, garlic, common sea buckthorn and others (Ng et al. 1987; Udintsev et al. 1991; Kasuga et al. 1999; Krylova et al. 2000). Table 1 Coefficients of rank correlation between abundance of food plants and faecal corticosterone, body mass and number of gerbils in colonies. Corticosterone [66] (April_May)b _0.11 0.12 _0.33* 0.03 a Food plants Ephemeral herbage (April_May) Perennial shrubs (May) Succulents (August_September) Haloxylon trees (September) a Body mass [48] (April_May) 0.44* 0.07 0.20 _0.06 Gerbil nos. [48] (May) _0.01 _0.11 0.05 _0.02 number of pairs; date of sampling; *P<0.05 b The number of pairs for corticosterone is higher than for body mass and number of colonies because 2_3 faecal samples were collected from 17 of the 48 males studied 18 Moshkin et al. As mentioned above, succulents become an appreciable part of the great gerbil diet in late May, but they also consumed succulent sprouts which appeared in late April. If these sprouts have any bioactive compounds that influence the HPA axis, the abundance of sprouts could correlate with corticosterone in gerbil faeces collected in the spring and, as a secondary effect, a relationship could be found between corticosterone and future abundance of the mature plants. According to this hypothesis, a correlation between corticosterone and succulents should show a definite increase at the time when succulents begin to sprout. To check this assumption, we recalculated the correlations between faecal corticosterone and succulents by means of successive subtractions of data beginning from the first day of sampling. From April 1 to April 25 the correlations were in the range of 0.23 to 0.39 and were not significant (Figure 6 and Figure 6A), but at the end of April their values increased dramatically just at the time when succulents began to sprout (Figure 6). The significant inverse relationship for the period April 26 to May 7 between faecal corticosterone content and abundance of succulents (Figure 6B) may be because the new growth of these plants contains compounds that inhibit HPA activity. Body mass of adult males trapped after April 25, however, did not correlate with abundance of succulents (r = 0.30, n = 15; P>0.05) and the positive relationship of mass with spring ephemerals (r = 0.57, n = 15; P<0.05) showed that grasses still constituted the main food source in late April and early May. Spring stress in fathers and survival of offspring If the relationship between HPA activity and succulents was formed by plantherbivore coevolution, what is the adaptive meaning of the stress response to shortage of the succulent sprouts? An increase in spring of faecal corticosterone in adult males is associated with an increased mortality in the summer (Rogovin et al. 2003) and stress for fathers might benefit their progeny. Stress induced mortality of adult males as a speciesspecific adaptation to environment with scarce food was described for the marsupial mice Antichinus stuiarty (Bradley et al. 1980). Males of this species die just after the breeding season and their death facilitates the survival of the pregnant females and offspring due to reduction of competition for food. We calculated survival of juveniles during the summer drought in colonies of great gerbils that were categorized as three types of family groups: groups in which the adult male survived (group I), those in which the adult male did not survive (group II), and those in which neither the adult male nor the adult females survived (group III). Survival of juvenile gerbils was similar in these groups (Table 2). Since survival rate (SR) depended on the abundance of succulents, as described by highly significant linear regression (SR = 11.9 + 162[log(succulent + 1)]; F1,40 = 13.4; P<0.001), we reconsidered survival of juveniles in colonies that occupied areas where abundance of succulents was less thaen the upper limit in the colonies Figure 6 Change of correlation coefficient between abundance of succulents and male faecal corticosterone after consecutive subtraction (day by day) of data collected from April 1 to May 7. Relationship between succulents and concentration of