Behavioral Ecology Advance Access originally published online on February 16, 2005
Behavioral Ecology 2005 16(3):606-613; doi:10.1093/beheco/ari033
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Maternal rank is not correlated with cub survival in the spotted hyena, Crocuta crocuta
Museum of Vertebrate Zoology, 3101 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA
Address correspondence to P.A. White, who is now at 642 Pheasant Ridge Road, Monterey, CA 93940, USA. E-mail: paw{at}carnivoreconservation.com.
Received 21 March 2004; revised 7 November 2004; accepted 17 January 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Reproductive success in female spotted hyenas, Crocuta crocuta, is positively correlated with social rank. High-ranking females are known to produce more offspring, but the effects of maternal rank on early cub survivorship have not been investigated. Cub mortality was examined over a 4-year period in one clan of wild-living spotted hyenas in Kenya. Data were obtained for 100 cubs in 63 litters produced by 27 adult females. Survivorship of cubs from birth through their first year was examined as a function of litter size, sex of cubs, and maternal rank. Overall, cub mortality was high (61%). Contrary to expectation, singleton cubs did not survive better than twins, and there was no difference in survivorship between female and male cubs. High-ranking mothers were not more successful at raising twins or daughters than were low-ranking mothers. There was no correlation between cub mortality and maternal rank. Peaks in cub mortality coincided with life stage events, including mean age of arrival at a communal den, and age at which cubs began visiting kills. Documented causes of mortality included intraclan infanticide, disease, orphaning, predation by lions, and a mechanism of filial infanticide that has not been previously described in this species: selective litter reduction by mothers via partial litter abandonment. No instances of facultative or obligate siblicide were detected. During this study, association between rank and number of cubs surviving to 1 year of age appeared to be due to differences in reproductive output and not differential survival of cubs within their first year.
Key words: Crocuta, infanticide, mortality, neonate, rank, siblicide.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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For the spotted hyena, Crocuta crocuta, social rank exerts a powerful influence over multiple aspects of an individual's behavior and life history. In adult females, this includes a strong positive correlation between rank and reproductive success (Frank et al., 1995a
; Hofer and East, 2003; Holekamp et al., 1996). Until now, differences in female reproductive success have been attributed mainly to fecundity. High-ranking females begin breeding at a younger age, have shorter interlitter intervals, and, thus, produce more offspring than lower-ranking females. Consequently, high-ranking females recruit more offspring to the age of sexual maturity than do low-ranking females (Frank et al., 1995a; Hofer and East, 2003; Holekamp and Smale, 1998; Holekamp et al., 1996).
These previous studies have focused on maternal rank as it relates to nutrition and examined survivorship of older cubs (3–12 months) and subadults (12–24 months). In contrast, the effects that variables such as litter size and cub sex may have on cub survivorship have not been thoroughly examined. Because causes of mortality change with age (Golla et al., 1999; Haas et al., 1996; Mills, 1990), rank may prove a more effective tool against protecting cubs from some threats than against others. Further, it is widely recognized that data on all aspects of neonatal (0–3 months) mortality are lacking (Frank et al., 1995a; Golla et al., 1999; Hofer and East, 1995). Discussions of obligate neonatal siblicide in Crocuta (Frank et al., 1991; Hofer and East, 1997; Smale et al., 1999) render analytical data on neonatal mortality of particular interest.
Maternal rank is hypothesized to play an important role in cub survivorship for two main reasons. First, rank is positively correlated with access to food (Frank, 1986b; Henschel and Skinner, 1987; Tilson and Hamilton, 1984). High-ranking females obtain more resources and consequently provide better nourishment for their cubs through lactation (Gittleman and Oftedal, 1987; Hofer and East, 2003; Oftedal and Gittleman, 1989). As a result, cubs of high-ranking female Crocuta are weaned earlier (Holekamp and Smale, 1995) and grow faster (Hofer and East, 2003) than cubs of low-ranking females. Among Serengeti cubs, the growth rate during the first 6 months of life was in turn linked to cub survival to the age of adulthood (Hofer and East, 2003). Mothers also allow their own cubs to feed with them at kills (Tilson and Hamilton, 1984). Thus, high rank is equated with superior nutrition to offspring, both through lactation and access to solid food. Second, rank dictates the outcome of dyadic encounters with conspecifics (Frank, 1986b). High-ranking females dominate aggressive encounters, potentially allowing them to better defend their cubs from conspecific threats. Therefore, for reasons relating to both nutrition and defense, maternal rank is expected to show a positive correlation with cub survivorship.
Other factors, such as the presence of a sibling and sex of a cub, may represent significant variables in terms of cub survivorship. Siblings necessitate a division of maternal resources (Loveridge, 1986; Oftedal, 1985), with the result that singletons grow faster than twins (Hofer and East, 1993). Therefore, singletons may be more likely to survive than twins regardless of their mother's rank. Sex of cubs may also differentially affect cub survivorship, particularly if male and female cubs differ in their nutritional requirements. Spotted hyenas are sexually dimorphic, with females weighing more than males as adults (Kruuk, 1972). Growth rates of cubs within their first year are higher for females than for males (Drea CM, Coscia EM, Weldele ML, Frank LG, and Glickman SE, unpublished data). Therefore, raising a daughter may be initially more expensive than raising a son. Thus, the superior nutrition available to high-ranking mothers may allow them to be more successful than low-ranking mothers at raising twins or daughters.
Within this clan, high-ranking females have previously been found to produce more offspring compared to low-ranking females (Holekamp et al., 1996). That study, however, did not assess mortality of neonates housed in natal dens. Moreover, the majority of data were collected after the arrival of cubs to a communal den. Cub production by low-ranking females may have been underestimated if neonatal mortality among cubs belonging to low-ranking females was high. By comparison, the present study examined cub production (litter sizes) and mortality from as early as the day of birth. Because this study included neonates and because productivity may vary over time, it was necessary to reexamine the relationship between rank and productivity over the time period of this study.
The goal of this study was to investigate whether differences in productivity alone could account for the higher reproductive success previously reported for high-ranking female Crocuta or if cub mortality was also correlated with maternal rank. Specifically, I predicted that while (1) cub productivity would be higher among high-ranking females, (2) cub mortality would be lower among high-ranking females, for example, cub mortality would show a negative correlation with maternal rank. Additionally, because nutrition affects maternal condition and lactation, (3) high-ranking mothers should be more successful than low-ranking mothers at raising twins, while (4) across ranks, singletons should survive at a higher rate than cubs in twin litters. Moreover, due to the apparently higher investment required, (5) high-ranking females should be more successful than low-ranking females at raising daughters. As described above, higher-ranking females are expected to be better able to defend their cubs against aggressive conspecific interactions. Therefore, I examined the age at which cubs died to see if the patterns were consistent with either the obligate neonatal siblicide hypothesized to occur in this population (Frank et al., 1991), the facultative siblicide (enforced starvation) (Hofer and East, 1997) that accounts for the majority of mortality among Serengeti cubs, or other sources of cub mortality associated with specific life stages (Holekamp and Smale, 1998), for example, arrival of cubs to a communal den. To test these predictions, I examined the survivorship of cubs to the age of 1 year, with special focus on the period from birth to 3 months of age when births and early losses would have been most likely to go undetected in prior studies.
Neonatal mortality has been little studied in Crocuta due to inherent difficulties in locating, sexing, and distinguishing between newborn siblings. Thus, I employed a variety of techniques, including the novel use of a remotely operated "burrow probe" camera system, to overcome these problems and to report on litter sizes, sex ratio, and mortality among neonates from as early as the day of birth.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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This study was conducted from November 1993 to December 1997 in the Masai Mara National Reserve (MMNR), Kenya, on one clan of hyenas previously studied by Frank (1986a
,b). This clan had been studied continuously since 1978, with the result that the genetic relationships among all adult and subadult females, as well as reproductive histories, were definitively known. Because these data were obtained from a single clan, however, results may be idiosyncratic to that clan. Individual Crocuta were recognizable by their unique spot patterns. During the current study, the number of adult (
2 years old) females in the clan fluctuated from 24 to 28 individuals due to adult deaths and juvenile recruitment.
Hierarchical rank of adult females was determined by observing the outcome of dyadic interactions using the same criteria as past investigators (Frank, 1986b; Holekamp and Smale, 1990, 1993; Smale et al., 1993). Unless otherwise noted, female rank refers to the absolute rank of females numbered from highest (1) to lowest (34) at time of parturition in relation to all other clan females 1 year old. Although females do not attain sexual maturity until a minimum of 2 years of age, subadult females (1–2 years old) routinely visit communal dens and interact with other adult females. Subadult female Crocuta are often aggressive towards lower-ranking adults (Frank, 1986b; Holekamp et al., 1993). Therefore, it was pertinent to include subadult females (n = 6) when calculating maternal rank. Where noted, mean ranks were calculated for each female by averaging her absolute ranks at the time of parturition for each litter. The term "cub" here refers to animals 0–12 months of age. Cubs were defined as "neonates" from the period 0–3 months of age.
For some analyses, mothers (n = 21) were assigned to rank categories to allow for stronger statistical analyses. Because matriline strongly influences social interactions (Frank, 1986a; Holekamp et al., 1997), category assignments corresponding to matrilines provided a biologically significant division and were used for all analyses involving rank categories. Rank category assignment followed that of previous studies; the high-ranking category contained only animals within the top-ranking (alpha) matriline, and the remaining matrilines (n = 8) were divided evenly between mid- and low-rank categories (Frank et al., 1995a). Mean age of females at time of parturition was 6.2 ± 3.3 years (n = 27 females, range 2.5–13.5 years). The mean age was not significantly different between the three rank categories (high: X = 5.2 ± 3.1 years, n = 21 litters from 7 females; mid: X = 6.2 ± 2.9 years, n = 25 litters from 13 females; low: X = 7.3 ± 3.9 years, n = 17 litters from 7 females) (ns ANOVA F2,60 = 2.10, p > .13). Nonetheless, mothers' age was used as a covariate in analyses of maternal rank on cub productivity and survivorship.
Locating neonates and determining litter size
Adult female spotted hyenas (n = 17) were anesthetized using Telazol (2.5 mg/kg) administered via Telinject rifle (Telinject, Agua Dulce, California, USA) and fitted with radio collars (Telonics, Inc., Mesa, Arizona, USA) to facilitate locating them at secluded natal dens. Radio-collared females were relocated via omni and H-antennae mounted to the front of a vehicle and a Telonics TR scanner-receiver. Uncollared females (n = 11) were located opportunistically at kills and during daily drives through the study area and followed to natal dens.
Mothers often picked up their newborn cubs and repositioned them on the rim or within the den opening, allowing for direct observations of cubs as early as the day of birth. In addition, a miniaturized infrared camera (FieldCam Basic System with a Burrow Probe III; Fuhrman Diversified, Inc., Seabrook, Texas, USA) mounted onto a remotely operated four-wheel drive platform was used to document litter size shortly after birth (range, 2–11 days) to quantify wounding on cubs and to search for dead cubs in burrows (White, 2002). Thus, while it is possible that cubs born dead or those dying within the first week might have been consumed by the mother and thus gone undetected, early detection of females at natal dens, intensive observer effort, and probe technology allowed determination of litter size at an earlier age than previously possible.
Distinguishing between neonates
After initial detection of a natal den, observations were performed twice daily (dawn and dusk) by an observer using a window-mounted Bushnell 20x spotting scope and 10 x 40 Leitz binoculars from within a vehicle parked 15–25 m from the den. Neonates spent most of their time inside the den and thus out of view, although they occasionally emerged as early as the day of birth for short periods of time. Additionally, mothers often picked cubs up out of the hole and carried them to the rim to nurse, and thus direct observations of cubs were possible even at the deepest dens.
Siblings were distinguishable through small and often subtle clues. Although uniformly dark at birth, neonates often showed differences in pelage sheen or hue, overall size, or morphology. Within the first week after birth, the cubs' ears began to stand erect, and ear shape was often unique. By week 2, scabs resulting from sibling aggression or mouthing by the mother and bare patches on the carpals from crawling in the burrows became apparent. At 6–8 weeks, distinctive patterns of white molt appeared around the cubs' eyes. By 10–12 weeks, permanent spot patterns become visible on the neck and anterior portions of the shoulders. From this age on, appearances continued to diverge and distinguishing between siblings became much easier. An overlapping chronology of these traits provided continuity in identifying individual cubs throughout the neonatal period. Spot patterns are both unique and permanent. A photographic file of all cubs was updated every 2–3 weeks as a reference in identifying individuals throughout their first year.
Sexing cubs
Female spotted hyenas have masculinized genitalia including an erectile phallus (Matthews, 1939; Neaves et al., 1980), making it difficult to sex cubs visibly. Prior to 3 months of age, the glans is still enclosed within the prepuce so shape cannot be seen (Frank et al., 1990). However, sexual differentiation in genital morphology is quantifiable in neonates <3 months of age (Forger et al., 1996; Glickman et al., 1998; White, 2002). The smoothed contour of the enclosed glans shows sexual dimorphism in shape as follows: males show greater taper at the tip, while the tip of the females' phallus is square in shape. Additionally, a male's phallus is relatively longer than that of a female. Both differences are phenotypically distinguishable from birth, and cubs younger than 3 months old can be reliably sexed using these characters. Comparisons of early assignment of cub sex using the relative length and shape method described above to sex of the same cub as determined either after 3 months of age (if the cub survived) (n = 50) or by presence of testes or uterus during necropsies of cubs that died (n = 11). In all cases where comparisons were possible (n = 61 cubs comprised of 27 females, 34 males), sex as determined 
3 months of age agreed with sex as determined later (White, 2002).
Determination of cub mortality
Cause of death was determined through necropsy of cub remains (n = 12) or observations of predation events (n = 3). Additionally, dependent cubs were considered to have died if they permanently disappeared from the natal territory (n = 46). Female spotted hyenas remain in their natal clans for life, and males are not expected to disperse until after reaching sexual maturity at the age of 24 months (Frank, 1986a).
Causes of mortality were related to life stages adapted from Holekamp and Smale (1998), and defined as follows. Stage 1: birth to approximately 4 weeks of age, during which time cubs are typically housed in a private, natal den. Stage 2: the period from approximately 4 weeks to approximately 4 months of age when cubs are typically housed in a communal setting, the location of which is determined by their mother. Stage 3: from 4 months to 1 year of age, when cubs are still largely dependent on their mother's milk, but also spend time away from the communal den on their own or in the company of other members of the clan.
Independence of samples
Data were obtained for 63 litters produced by 27 adult (2 years old) females. During this study, each adult female in the clan gave birth to from one to five litters (X = 2.4 ± 1.1 litters), with the exception of one additional adult female who did not breed. Primiparous females may suffer disproportional cub mortality due to the anatomical difficulties of giving birth through a phallus (Frank et al., 1995b). Therefore, primiparous litters (n = 15) were examined separately from females' subsequent litters. The sole triplet litter detected presented a special case, as the lowest ranking cub (third) had two dominant siblings and therefore did not fall into the same category as all other "subordinate" twins. With the exception of analyses involving total number of cubs born and died, this third cub was excluded from all data sets. After the death of the third cub at 30 days of age, data generated from the remaining two siblings were included in subsequent analyses as a female/female twin litter.
For analyses involving maternal rank, data were analyzed in one of two ways: (1) with each litter treated as an independent data point with the absolute rank of the mother calculated at the time of parturition or (2) with each litter treated as an independent data point with mothers assigned to ranked categories. Measures of productivity were obtained on each female for which there were data on at least 3 years of reproductive life (n = 24). Annual cub production was calculated as the total number of cubs born divided by the number of years a female was present during the study after reaching 36 months of age, or after conceiving her first litter, if prior to 36 months of age. For these same mothers, annual cub survivorship was calculated as the total number of cubs surviving to the age of 1 year divided by the number of years the female was present.
Statistical analyses were performed using JMP 4.0.2 software. ANOVA (F) tests were used for comparisons of multiple means of the same variable. For analyses involving female reproductive performance, correlation coefficients (Spearman's Rs) were obtained to indicate whether cub production and survivorship varied with maternal rank after controlling for effect of maternal age. Student's t tests were used for all pairwise comparisons of means. Likelihood chi-square tests (
2) were used in testing categorical variables.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Maternal rank effects on cub production and mortality
The annual rate of cub production among MMNR females during the study period (1994–1998) was positively correlated with maternal rank (Rs = –.500, p = .015). High-ranking females gave birth to more cubs than did low-ranking females (Figure 1a).
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Cub loss, as total percentage of all cubs born to each female during the study, was assessed for the same set of females. In contrast to cub production, maternal rank had no observable effect on cub mortality to the age of 1 year (Rs = .148, p = .500) (Figure 1b).
Surviving cubs were distributed across all ranks (Figure 1c). The number of cubs surviving to 1 year of age was positively correlated with maternal rank (Rs = –.454, p = .029). Because high-ranking females produced more cubs, the number of survivors mirrored the trend in cub production, with high-ranking females averaging higher numbers of surviving cubs (X = 2.5 cubs/female). Mid- and low-ranking females raised on average the same number of offspring to the age of 1 year (X = 1.5 cubs/female).
Survivorship curve
A cumulative survivorship curve showed a steep decline in the percentage of cubs remaining through the first 9 months after birth (Figure 2). Although mortality continued to occur throughout the first year, the rate slowed around 8 months of age. The cumulative survivorship curve was well described by a nonlinear bivariate fit (F = 364.93, p = .0003).
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Survivorship curves from this and previous studies reporting on mortality in older cubs were generally consistent but with some important differences. By 3 months of age, mortality was significantly higher (
2 = 14.07, df = 1, p = .0002) than reported for this MMNR hyena clan over a different time period (Frank et al., 1995a). Overall, this study documented higher mortality of cubs during their first year after birth (61%) than previously reported from the Serengeti ecosystem (Serengeti 53% [Hofer and East, 1995]; Masai Mara 50% [Frank et al., 1995a], with the steepest rate of loss occurring between the ages of 1 and 3 months.
Litter composition and sexes of cubs born and died
Sex differences in cub mortality mirrored cub production; all females lost cubs in roughly the same sex ratio in which they produced them (Figure 3). Low-ranking females gave birth to a significantly higher proportion of males than did either high- or mid-ranking females (2 = 9.76, df = 1, p = .001).
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Hypotheses regarding cub survivorship in relation to sex and litter size were not upheld. There was no significant difference in mortality among cubs in twins litters (40/70 = 57% mortality) compared to singletons (15/23 = 65% mortality) (
2 = 0.47, df = 1, p > .49). Although female cubs were the dominant siblings in 11 of 15 mixed-sex litters, female cubs in mixed-sex litters were no more likely to survive than their male counterparts (F: 10/15 = 67% mortality; M: 5/15 = 33% mortality). Overall, there was no difference in mortality of female and male cubs (F = 53%; M = 50%) (2 = 0.06, df = 1, p > .80).
Cub age at death
Maternal rank had no significant effect on mean cub age at death (high rank X = 15.7 ± 12.3 weeks, n = 20 cubs from 7 females; mid rank X = 16.8 ± 13.3 weeks, n = 26 cubs from 12 females; low rank X = 12.4 ± 9.5 weeks, n = 14 cubs from 6 females) (F2,57 = 0.60, p > .55). Analysis of cub mortality by life stage, however, found that low-ranking females lost more cubs during the first life stage (0–1 month of age) (Figure 4). Low-ranking females were the only mothers to lose a greater percentage of offspring in the first month than in the following period. By comparison, mid and high-ranking mothers suffered greater losses of older cubs. Among females of all ranks, cub death in the third life stage represented the highest proportion of cub loss during the first year.
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Mean age at death for all cubs (n = 60) was 15.4 ± 12.1 weeks. Among cubs of known sex, mean age at death did not differ significantly for females (21.5 ± 10.8 weeks, n = 19) and males (19.1 ± 12.6 weeks, n = 22) (t39 = 0.66, p > .51). Peaks in cub mortality appeared to coincide with risk factors related to specific life stages (Figure 5). Mortality peaks occurred immediately after (1) the age at which cubs first arrived at a communal den, (2) the age at which cubs first spent time away from the protection of a communal den (especially overnights), and (3) the age at which cubs first began visiting kills.
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Primiparous litters
Fifteen primiparous litters composed of an equal proportion of singletons and twins (7:7, + 1 unknown composition) were born during the study. In captivity, primiparous litters are often stillborn due to difficulties associated with giving birth through a phallus (Frank et al., 1995b
). In the wild, stillborn cubs would likely have been consumed by the mother prior to detection, which may have biased the proportion of singletons to twins. However in this study, primiparous litter sizes did not differ from those of parous females (2 = 0.49, df = 1, p > .48), although sample sizes were small. There was no significant difference in percentage of mortality among cubs in primiparous litters (76%, n = 15) and those born to parous females (2 = 1.82, df = 1, p > .18).
Causes of cub mortality
Two previously undocumented causes of cub mortality were observed: (1) infanticide by lower-ranking clan females (n = 2) and (2) selective parental infanticide (n = 3) (Mock and Parker, 1997). Other causes of cub mortality documented during this study included starvation after orphaning (n = 9), disease (n = 1), injury (n = 1), inclement weather (n = 1), humans (hit by car) (n = 1), and interspecific predation (n = 1). Specific risks appeared to change over time, in accordance with life stages.
A dramatic instance of infanticide was observed when a female transported her day-old cubs to a communal den, nursed them there all morning, and then left the cubs for the remainder of the afternoon. Prior to the mother's return, another adult female (a full sister to the new mother) arrived and methodically killed both newborns with crushing bites to the head. On three other occasions, I observed adult females consuming neonates at communal dens. In each instance, the cubs had been transferred to the communal den <3 days before and had been seen to be in good condition the prior evening. Two additional litters disappeared under suspicious circumstances when new mothers moved their cubs to communal dens comprising a sister and her own litter. The next day when the new mother returned, the sister was present but the new cubs were gone. In contrast, although immigrant males were often seen visiting cubs at communal dens in the absence of adult females, there was no evidence to support infanticide by males.
In three litters, young cubs (aged 5.5, 7.0, 10.5 weeks) were permanently abandoned by their mothers in acts of selective parental infanticide (Mock and Parker, 1997). In each instance, the mother was a low-ranking female who had given birth to male twins. Between 6 and 8 weeks of age, sibling competition during nursing bouts by these twin pairs intensified (White PA, personal observations). Prior to abandonment, mothers attempted to decrease sibling conflict by temporarily separating cubs, either by carrying one cub away from the den to nurse or housing cubs in separate dens. However in each instance, the subordinate twin was ultimately abandoned when the mother either moved the dominant cub to a new den (n = 2) or transported the subordinate cub to a remote, private den (n = 1). In both scenarios, the mothers were not known to return to their subordinate cubs that subsequently died of starvation.
Five litters of dependent cubs died of starvation as a result of orphaning. Cubs as old as 7 months (n = 4) were observed to starve after their mother's death. This included cubs belonging to high-ranking females, who were presumably well nourished at the time of their mother's death. In no case was an orphaned cub observed to be suckled or adopted by other females, even though four of the five litters belonged to large matrilines, and at least some orphaned cubs had relatives who were currently lactating.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Observed patterns of cub mortality were not consistent with hypotheses relating to maternal resource limitations. There was no difference in mortality between cubs in singleton versus twin litters or between female and male cubs. The fact that singletons did not survive better than twins is particularly intriguing and suggests that the presence of a sibling may in some way prove advantageous to cub survival, especially when cubs first begin to wander from the communal den. Cooperation among Crocuta siblings increases dramatically after the cessation of early aggression (Smale et al., 1995
). Smale et al. (1995) hypothesized that the associative behavior of siblings may prove advantageous in coalition formation, thereby enhancing juvenile survival. Likewise, the present findings suggest that in the absence of resource limitations the presence of a sibling may improve a cub's chance of survival in the first year of life.
Maternal rank showed no correlation with cub mortality. High-ranking females successfully reared greater numbers of cubs to the age of 1 year due to the fact that they gave birth to greater numbers of offspring. This result is surprising given that rank profoundly influences an individual's access to food resources (Frank, 1986b; Henschel and Skinner, 1987; Tilson and Hamilton, 1984) and is further evidence that, during the course of this study, resources did not play a significant role in cub mortality. The exception was three cases of selective parental infanticide (Mock and Parker, 1997), where low-ranking mothers were presumably unable to support twins. In these cases, subordinate cubs were at times deliberately abandoned. Similarly, in Serengeti where resource limitations frequently result in starvation of older cubs, it is the subordinate sibling that perishes (Hofer and East, 1993). If resources constituted the primary cause of cub mortality in MMNR, however, starvation of the subordinate cub would be the expected outcome; thus, dominant siblings should out-survive littermates of either sex. Yet in several instances during the course of this study, dominant siblings in twin litters died while their subordinate littermate survived (White, 2002).
Prey availability has been shown to influence cub survival in the Serengeti where mothers must commute long distances in search of food (Hofer and East, 1993). In that system, low-ranking mothers traveled longer distances, a strategy that necessitated prolonged absences from their cubs compared to high-ranking females (Hofer and East, 1993). Consequently, cubs of low-ranking females grew slower and showed more intralitter aggression over resources (Golla et al., 1999). In MMNR, cubs are rarely food stressed, and thus mortality patterns may differ from hyenas in other systems. Although prey abundance in MMNR fluctuates seasonally and annually (Holekamp et al., 1993), year-round prey availability is high enough to allow for mothers of all ranks to return daily to nurse their offspring (White, unpublished data). Similarly, Wachter et al. (2002) reported low levels of intralitter aggression among cubs in Ngorongoro where prey is abundant. Studies focusing on the fate of young cubs in ecosystems where resources are less abundant would be of interest in testing whether maternal rank effects on neonatal mortality become apparent under more extreme conditions.
The percentage of cub mortality was conspicuously high among mid-ranking females. Previously, researchers have noted elevated conflict associated with beta (mid) ranks in this species (Zabel et al., 1992). Here, the observed and suspected cases of intraclan infanticide occurred among mid-ranking females. Although some low-ranking females successfully raised a large proportion of their litters, low-ranking females had greater variability in their success of raising cubs to 1 year of age.
Maternal rank did influence the age at which cubs perished. Cubs of low-ranking females died at younger ages than cubs belonging to higher-ranking females. This included three litters where cubs were selectively abandoned. In the face of adverse resource conditions, early litter reduction may be the best strategy for low-ranking mothers who find themselves unable to support twins, as consolidating their resources should improve the chance of survival for the remaining cub. In contrast, mid-ranking and high-ranking mothers are better able to nourish twins during periods of low prey abundance, after which a sudden increase in resources can result in rapid improvement of maternal condition and in turn, increased chance of cub survival.
This study commenced immediately after an outbreak of canine distemper virus (CDV) in the Serengeti/Mara ecosystem (Alexander et al., 1995; Haas et al., 1996). A single cub in this study for which disease was listed as cause of death exhibited the symptoms associated with CDV in Crocuta (Haas et al., 1996), although the presence of CDV was not verified in that cub. No other cubs in this study were observed to exhibit symptoms of CDV, although it is possible that some of the cubs that perished from "unknown" causes succumbed to this disease. In addition to other stochastic factors (e.g., weather), diseases would be expected to indiscriminately affect cubs of all ranks.
Although this study found no significant effect of rank on mortality of cubs during their first year, rank effects may require longer-term studies to show patterns or may take longer to manifest within individuals. Previous studies of rank and reproductive success (e.g., recruitment of cubs to sexual maturity) that reported no significant correlation over a short timescale (Frank, 1986b) subsequently found rank to have a significant effect when examined over a longer time period (Frank et al., 1995a). In chimpanzees, Pan troglodytes, Boesch (1997) found that the effect of maternal rank on survivorship of sons became statistically significant only after the offspring reached 5 years of age.
Peaks in cub mortality corresponded to life stage events. The first of these peaks coincided with the age (approximately 1 month) at which cubs typically arrived to the communal den. Observed and suspected instances of infanticide occurred after successful transfer of cubs to communal dens. Further, the majority of young cubs that died of unknown causes disappeared suddenly after sightings of them as healthy individuals after their arrival at the communal den. Some social restraint to infanticidal behavior must exist, as communal denning would not persist were cubs routinely killed by other clan members. Moreover, clan size is positively correlated with competitive success at kills against both lions and other hyena clans (Kruuk, 1972). Nonetheless, the observed incident and the repeated instances of cub disappearances that entailed suspicious circumstances support the suggestions of past researchers (Frank et al., 1995a; Hofer and East, 1995; Mills and Hofer, 1998) that infanticide may contribute substantially to neonatal mortality in this species.
It is now apparent that even close relatives (e.g., full sisters) may at times kill each other's cubs and that infanticide may operate irrespective of rank. Although infanticide has long been suspected in this species (Hofer and East, 1995; Kruuk, 1972), prior to this study, infanticide by lower-ranking clan females against higher-ranking cubs had not been documented. Intraclan infanticide in Crocuta is consistent with predictions from the local resource competition hypothesis (Clark, 1978; Silk, 1983), which states that, at least in some instances, removal of a future competitor may prove more advantageous than addition of a relative to the matriline or clan. Although infanticide by close relatives is contrary to expectations based on inclusive fitness benefits (Hamilton, 1964), it has been reported or suspected among several species of carnivores (Packer and Pusey, 1984). For most social carnivores, permanent groups are composed of close kin (Clutton-Brock, 2002). Therefore, intragroup infanticide is likely to be perpetrated between close relatives. A growing body of literature points out that close kin may represent one's closest competitors (Hausfater and Hrdy, 1984; Hoogland, 1985; Hrdy, 1979; Mumme et al., 1983) and that elimination of a future competitor may be more genetically advantageous than altruistic behavior (Mock and Parker, 1997, 1998; Tuomi et al., 1997; West et al., 2002).
Although cub mortality was high throughout the first month, no evidence of obligate (Frank et al., 1991; Mock and Parker, 1997) or facultative (Hofer and East, 1993, 1995; James and Hofer, 1999; Mock and Parker, 1997) siblicide among Crocuta twins was detected. The obligate siblicide hypothesis states that the dominant cub inflicts wounds on the subordinate sibling and keeps the subordinate from nursing. The subordinate cub becomes progressively weaker due to infection and starvation and ultimately dies. Obligate siblicide is hypothesized to occur within a narrow time period consisting of the first month after birth (Frank et al., 1991). While it is possible that in this study deaths occurred in the first week of life prior to video probing of burrows, probes and sightings of litters were theoretically early enough to cover the siblicidal period. It is unlikely that starvation would occur within the first week after birth because, unlike most mammals, hyena cubs are evolutionarily designed to survive for considerable periods between nursing bouts (Hofer and East, 1993). Neonatal Crocuta are rapidly sated during nursing bouts (White PA, personal observations) and as a result even a low-ranking mother who may have less milk can successfully nurse two young cubs by staggering nursing times or by temporarily separating cubs (White, 2002). Thus, subordinate cubs are unlikely to face a life-threatening resource crisis until they are at least several weeks old.
In contrast, the facultative siblicide among Serengeti hyenas is resource based, with the dominant cub forcibly excluding its subordinate sibling from nursing resulting in a body size discrepancy among siblings and ultimately, death of the subordinate cub (Hofer and East, 1993, 1995, 1997). Even in the Serengeti where cub dependency on maternal milk is extended and facultative siblicide is the most prevalent known cause of cub mortality, the mean age at which cubs starved was X = 86 ± 70.5 days (n = 22), with a minimum recorded age of 12 days of age (Hofer and East, 1997). Apart from the orphaned and abandoned cubs described above, during the present study no cubs starved such as occurs in facultative siblicide.
The survivorship curve described an exponential rate of decline for cubs during their first year, closely resembling previous reports from the greater Serengeti ecosystem (Frank et al., 1995a; Hofer and East, 1995). However, this study documented a higher overall rate of mortality that continued until 8 months of age, with greater monthly fluctuation. Mortality rates may be influenced by stochastic events (e.g., droughts), and short-term weather patterns may have influenced the differences between studies. Alternatively, the more intensive coverage of the neonatal period reported herein might be a more accurate portrayal of early cub loss in spotted hyenas. Future efforts that combine intensive coverage of neonates with comparisons of cub mortality among different clans are needed to ascertain whether the level of cub mortality reported here is widely representative of the species.
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ACKNOWLEDGEMENTS |
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I thank the Office of the President of Kenya for permission to conduct this research (OP/13/001/C689; KPP No. 253151). The Kenya Wildlife Service, Narok County Council, and the Senior Warden of the Masai Mara National Reserve each contributed importantly to this effort. Field research was supported by National Science Foundation grant IBN-9306912. The National Institute of Health grant MH-39917 and the Annie M. Alexander California Museum of Vertebrate Zoology Scholarship provided additional financial assistance. Animal Use Protocols R191-1195 for animal handling were approved by the University of California, Berkeley's Animal Care and Use Committee. I am indebted to L. Frank for providing the opportunity to perform this research and P. Barber for his efforts in establishing this project. S. Glickman, E. Lacey, and W. Getz provided invaluable counsel throughout the course of this work. I thank I. Owens and two anonymous reviewers for their thoughtful comments and suggestions on earlier drafts of this manuscript.
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