Reproductive Success of Female Leopards Panthera Pardus: the Importance of Top-Down Processes Guy A

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Mammal Review ISSN 0305-1838

REVIEW Reproductive success of female leopards Panthera pardus: the importance of top-down processes Guy A. BALME* Panthera, 8 West 40th Street 18th Floor, New York, NY 10018, USA. E-mail: [email protected] Andrew BATCHELOR Mala Mala Game Reserve, Greater Kruger National Park, Skukuza, 1350 Mpumalanga, Republic of South Africa. E-mail: [email protected] Natasha DE WORONIN BRITZ Global Leopard Project, Erindi Private Game Reserve, PO Box 467, 9000 Omaruru, Republic of Namibia. E-mail: [email protected] Greg SEYMOUR Terra Nova Conservation Services, PO Box 463, Douglasdale, 2165 Gauteng, Republic of South Africa. E-mail: [email protected] Michael GROVER Sabi Sand Wildtuin, Greater Kruger National Park, Skukuza, 1350 Mpumalanga, Republic of South Africa. E-mail: [email protected] Lex HES PO Box 19113, Nelspruit, 1200 Mpumalanga, Republic of South Africa. E-mail: [email protected] David W. MACDONALD Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, The Recanati-Kaplan Centre, Tubney, Abingdon OX13 5QL, UK. E-mail: [email protected] Luke T.B. HUNTER Panthera, 8 West 40th Street 18th Floor, New York, NY 10018, USA. E-mail: [email protected]

Keywords ABSTRACT demographic determinants, kin selection, life history traits, long-term monitoring, mating 1. Long-term studies on large felids are rare and yet they yield data essential strategies to understanding the behaviour of species and the factors that facilitate their conservation. *Correspondence author. 2. We used the most extensive data set so far compiled on leopards Panthera pardus to establish baseline reproductive parameters for females and to determine Submitted: 13 December 2011 Returned for revision: 13 March 2012 the demographic and environmental factors that affect their lifetime reproductive Revision accepted: 23 May 2012 success. Editor: KH 3. We used comprehensive sightings reports and photographs from ecotourism lodges in the Sabi Sand Game Reserve, South Africa, to reconstruct life histories doi:10.1111/j.1365-2907.2012.00219.x for 44 female leopards that gave birth to 172 litters over a 32-year period. 4. Leopards appeared to exhibit a birth pulse; most litters were born in the wet season, particularly in December. Mean age at first parturition (n = 26, mean Ϯ standard error = 46 Ϯ 2 months, range = 33–62) was older than previously recorded, possibly due to elevated intraspecific competition. Average litter size was 1.9 Ϯ 0.1 (n = 140, range = 1–3) and declined with maternal age. Age of litters at independence (n = 52, 19 Ϯ 1 months, range = 9–31) was inversely related to prey abundance but did not affect the likelihood of recruitment of offspring. Interbirth intervals differed following successful litters (in which at least one cub survived to independence; n = 55, 25 Ϯ 1 months, range = 14–39) and unsuccessful litters (n = 46, 11 Ϯ 1 months, range = 4–36), as did the time taken to replace litters. 5. Variation in lifetime reproductive success was influenced mainly by differences in cub survival, which was related to maternal age and vulnerability to infanticide. Cub survival (37%) declined as females got older, perhaps because mothers relin- quished portions of their home ranges to philopatric daughters. Male leopards were responsible for many (40%) cub deaths and females appeared to adopt several

strategies to counter the risk of infanticide, including paternity confusion and displaying a period of reduced fertility immediately after a resident male was replaced. 6. Our results suggest that the reproductive success of female leopards is regulated primarily by top-down processes. This should be taken into account in management decisions, particularly when managers are considering the implementation of invasive activities such as legal trophy hunting.

INTRODUCTION is difficult to gauge the impacts that such human-mediated mortality may have on leopard populations. It is also Population persistence is ultimately a function of mortality impossible to estimate effective population size or model and reproduction (Caughley 1977). Studies on the repro- metapopulation dynamics, aspects of leopard biology that ductive biology of species are therefore fundamental to their are key to the persistence of the species (McCullough 1996). conservation (Holt et al. 2003). However, accurately quanti- In this paper, we use the most extensive data set so far fying reproductive parameters requires longitudinal data compiled on leopards to establish baseline reproductive collected over multiple generations (Clutton-Brock 1988). parameters for the species. We also assess the effects of Such data are rare, particularly for long-lived carnivorous demographic and environmental factors on reproduction. mammals. Among the 37 extant wild felid species (Hunter & Carnivore populations are typically regulated by top-down Barrett 2012), only lions Panthera leo (Packer et al. 1988), processes (e.g. natural enemies) or by bottom-up processes cheetahs Acinonyx jubatus (Kelly et al. 1998) and, to a lesser (e.g. resource limitation; Kissui & Packer 2004). Lions and extent, pumas Puma concolor (Logan & Sweanor 2001) and spotted hyaenas Crocuta crocuta kill leopards, potentially tigers Panthera tigris (Smith & McDougal 1991) have been limiting their reproductive output (Balme et al. 2009). studied for sufficient periods to produce reliable estimates Infanticide can similarly curtail population productivity, of reproductive success. Here, we present reproductive data especially if turnover rates among adult male leopards are collectedover32yearsonaprotectedleopardPanthera high (i.e. if resident males are frequently replaced; Balme pardus population in the Sabi Sand Game Reserve (SSGR), et al. 2009, Packer et al. 2009). Alternatively, prey availability South Africa. Previous studies on leopard reproduction can affect carnivore reproduction by influencing pregnancy (Bailey 2005, Balme 2009, Owen et al. 2010) relied on cross- rates, age at maturity and levels of inter- and intraspecific sectional surveys that suffer numerous weaknesses. Notably, competition (Tannerfeldt & Angerbjörn 1998, Schwartz they often fail to account for trade-offs that exist between et al. 2006). Food shortages can also affect offspring survival reproduction and survival (Moyes et al. 2006). They may through increased starvation and abandonment (Packer also be affected by short-term changes in the environment et al. 1988, Kelly et al. 1998). Several researchers have exam- or population dynamics, which can artificially elevate vari- ined the individual influences of these factors on carnivore ance in breeding success (Clutton-Brock 1988). By tracking reproduction (though not for leopards), but few have inves- the fate of female matrilines across generations, our study tigated their simultaneous effects, and the subject remains overcomes these weaknesses and provides novel insight on a source of debate (see Kissui & Packer 2004 for review). the reproductive ecology of a species that is increasingly In addition to fluctuating ecological forces, reproductive threatened (Henschel et al. 2008). success may vary with maternal age. In some felid species, Although resilient in the face of human pressure, leop- older, more experienced mothers have a higher likelihood of ards have been eradicated from an estimated 37% of their raising cubs to independence (Packer et al. 1998, Pettorelli historic African range, due mainly to loss of habitat, deple- & Durant 2007), but they can also suffer from the increased tion of natural prey and direct killing by people (Ray et al. energetic costs of rearing offspring (Logan & Sweanor 2005). Large numbers of leopards are killed because of the 2001). Age at primiparity and reproductive senescence also real and perceived threat they pose to livestock (Balme et al. partly determine the number of litters a female can produce 2009, St John et al. 2011). In addition, 12 African countries during her life (Schwartz et al. 2003, Zedrosser et al. 2009). are permitted by the Convention for the International Trade Accordingly, we calculate age-specific maternity rates for of Endangered Species to export a quota of leopard skins female leopards and estimate their lifetime reproductive procured through trophy hunting (the combined annual success (LRS). Our results enhance the understanding of quota for all countries is 2648; Balme et al. 2010). Without leopard biology and facilitate improved management of the reliable estimates on reproduction and recruitment rates, it species throughout its range.

METHODS mammals (with the exception of elephants Loxodonta africana; Thomas et al. 2008). Forty-five species of large Study area mammals (excluding rodents and bats) have been recorded on the SSGR, including the entire indigenous large carni- The SSGR (625 km2; midpoint: 31°29′ E, 24°49′ S) is situ- vore guild (Radloff & du Toit 2004). ated in the lowveld region of the Mpumalanga Province, South Africa (Fig. 1). It comprises 20 privately owned properties that have been managed collectively as a conservancy Data collection since 1961. There are no internal fences between individual The SSGR includes 21 lodges that run as high-end destina- properties, and the eastern boundary fence that separates tions for photographic safaris. Clients are taken on two the SSGR from the Kruger National Park was removed in game drives daily, in the early morning and late afternoon 1993. Hence, animals range freely across a protected land- (c. 0530–0930 and 1600–2000 h). Game drives are con- scape of >22000 km2. The prevailing vegetation is open to ducted by an experienced guide accompanied by a trained semi-wooded savanna dominated by Combretum, Termina- tracker. Charismatic species such as leopards are highly lia and Acacia species, interspersed with grasslands and sought after and guides maintain radio contact with each wooded grasslands. It is a semi-arid ecosystem characterized other to maximize the opportunity of locating such by a warm, dry winter from April to September and a hot, animals. Success rates are high; clients at lodges viewed at humid summer from October to March, which includes the least one leopard on 337 Ϯ 15 (mean Ϯ standard error) rainy season. Average annual rainfall is 650 mm and mean days per year during the study (range = 310–363). Because monthly temperatures range from 19 to 33 °C. Numerous of the high number of vehicles active in the SSGR and its waterholes have been created to supplement the two peren- long history of protection, leopards have become habituated nial rivers that flow through the SSGR. Consequently, to the presence of game drives. As a result, guides are famil- there is little seasonal fluctuation in populations of wild iar with the leopards that use their traversing area (individuals can be distinguished by their unique spot patterns; Miththapala et al. 1989) and have been able to monitor their fates over time (see Hes 1991, Hancock 2000, Kure 2003). Guides from all lodges are required to record daily sightings of leopards, although the frequency of reporting varies. Owners of some lodges require guides to transcribe detailed ecological information (e.g. location of individuals, preda- tory behaviour and social interactions) after every game drive, while others simply require significant reproduction and mortality events to be recorded. The oldest records date back to 1979, but consistent reporting throughout the SSGR has taken place from 2000 onwards. We collated all long- term sightings records from the lodges and used these to reconstruct life histories of individual leopards in the SSGR. Female leopards are philopatric (Bailey 2005) and were thus likely to remain in the study area for their entire life. Conse- quently, we have far more complete data for females than for males, which often dispersed away from the SSGR (G. A. Balme, unpublished data). The home ranges of individual leopards usually overlapped the traversing area of game drives from several lodges (n = 44, mean = 4.1 Ϯ 0.3 lodges, range = 1–7), which allowed us to evaluate the consistency of reports. There was no discrepancy in the number of litters reported for individual females or in the fate of litters, but the recorded timing of events sometimes differed (although never by more than four months). In such cases, we used the median date between records. To ensure that Fig. 1. Map of the Sabi Sand Game Reserve study area (pale grey; maternity of litters was correctly assigned, we collected showing internal property boundaries) in relation to the Kruger photographs taken by guides of females together with National Park (dark grey), South Africa (hatched area in inset map). their offspring. In total, we amassed >3500 photographs

Mammal Review 43 (2013) 221–237 © 2012 The Authors. Mammal Review © 2012 John Wiley & Sons Ltd and The Mammal Society 223 Female leopard reproduction G. Balme et al. that included 85% of cubs that survived to independence Table 1. Baseline reproductive parameters for female leopards (n = 118). By using reports from multiple sources and con- Panthera pardus in the Sabi Sand Game Reserve, South Africa, firming the identity of individuals through photographs, we 1979–2010. Successful litters were defined as those in which at least one cub survived to independence were confident of the veracity of our data. Parameter N* Mean SE SD Min Max Reproductive parameters Age at first parturition 26 46 2 8 33 62 (months) We used sightings records collected by guides between Litter size 140 1.9 0.1 0.6 1.0 3.0 January 1979 and December 2010 to estimate the following Age of litter at independence 52 19 1 5 9 31 reproductive parameters for female leopards: age at first (months) parturition, litter size, age of the litter at independence and Interbirth interval after 55 25 1 7 14 39 successful litters (months) interbirth intervals for successful and unsuccessful litters. Interbirth interval after 46 11 1 6 4 36 We defined successful litters as those with at least one cub unsuccessful litters that survived to independence. Age at primiparity was only (months) estimated for known-age females (i.e. those first observed as *Sample size. cubs under four months old). Litter size in our study was Max, maximum estimate; Min, minimum estimate; SD, standard devia- determined earlier (n = 140, mean = 49 Ϯ 4 days after birth, tion; SE, standard error. range = 1–270) than previously documented (Bailey 2005, Balme 2009, Owen et al. 2010), but it still represents a minimum estimate as some cubs may have died prior to right-censored individuals still alive at the end of the study. detection. Interbirth intervals were only calculated for The Kaplan–Meier method assumes that survival times females seen on at least a monthly basis and for litters first are independent among individuals (Pollock et al. 1989); observed when under four months old. This reduced the however, siblings were frequently killed in the same inci- chances of excluding litters that died at an early age and dent. Hence, we also calculated litter survival to 18 months. ensured that errors associated with our interbirth interval We used log-rank tests to compare survival curves of male estimates were negligible. Young leopards were considered and female cubs and of cubs born during the wet and dry independent when they were no longer seen associating seasons (Pollock et al. 1989). with their mothers. However, individuals that disappeared The causes of cub mortality were not always apparent. We suddenly at a young age were excluded from the analysis only included records in which the actual mortality event because they were likely to have died (newly independent was observed or could be unambiguously determined by leopards were typically observed in their natal area for post-mortem and evidence collected at the site. We calcu- several months before they dispersed; G. A. Balme, unpub- lated the mean proportions of litters lost and the average lished data). Age at independence was estimated for litters age of cubs affected by the different sources of mortality. rather than cubs, as mothers typically left siblings at a similar time. To determine if age at independence affected Reproductive success recruitment, we established whether individuals survived to breeding age. Subadults that dispersed from the study area Past studies of leopard reproduction included only breeders before 46 months (mean age at first parturition; Table 1) in estimates of fecundity (Balme 2009, Owen et al. 2010), so were censored. the reproductive potential of populations is likely to have Data were also extracted on the copulatory behaviour of been overestimated (Clutton-Brock 1988). We calculated leopards. We calculated the length of consortships (though age-specific fecundity as the number of offspring born to this was a minimum estimate as mating may have begun females in a particular age class divided by the total number before and continued after leopards were encountered), the (breeders and non-breeders) of females monitored in that frequency of consortships and the number of different age class (Packer et al. 1998). In this way, we estimated males that females were observed mating with between suc- maternity rates for the entire population. We estimated cessive litters. female survivorship to determine whether reproductive senescence occurred before maximum longevity. We also calculated the LRS of female leopards with com- Cub survival plete reproductive histories (i.e. those monitored from birth We used the Kaplan–Meier method (Pollock et al. 1989) to until death). LRS is generally considered the sum of all estimate age-specific survivorship for all cubs born during recruits produced by an individual in its lifetime (Clutton- the study. We assigned the median litter size of two to Brock 1988). However, data on the number of leopards litters that disappeared before cubs could be counted and reaching breeding age were incomplete; hence, we used the

224 Mammal Review 43 (2013) 221–237 © 2012 The Authors. Mammal Review © 2012 John Wiley & Sons Ltd and The Mammal Society G. Balme et al. Female leopard reproduction number of cubs reaching independence as the metric of guides submitted estimates of the lion and leopard popula- LRS, acknowledging that this is an overestimate. We applied tions using their traversing area to the SSGR management the model developed by Brown (1988) to assess the relative based on the numbers of known and unknown individuals importance of the different components of LRS (reproduc- that they viewed (Sabi Sand Wildtuin, unpublished data). tive longevity, fecundity and cub survival). To allow com- We used these estimates as measures of inter- and intraspe- parison with other studies, we restricted our analysis to ciﬁc competition. They are relatively coarse indices of abun- females that raised at least one cub to independence. dance; however, sampling effort (the number of game drives active) remained constant throughout the study period 2 (c 7 = 5.469, P = 0.603), as did the number of sightings per Correlates of reproductive success 2 season (c 7 = 0.750, P = 0.993) and the ratio of known to 2 We used the Kullback–Leibler information-theoretic unknown leopards observed (c 7 = 11.910, P = 0.104). Lion approach (Burnham & Anderson 2002) to test the effects of and leopard numbers were negatively correlated (Pearson’s different demographic and environmental covariates on correlation coefﬁcient =-0.776, n = 8, P = 0.024) and were litter size, age of litters at independence and reproductive thus excluded from the same analyses. For models relating success (i.e. the likelihood of at least one cub surviving to to reproductive success, we included a dichotomous covari- independence). For each analysis, we constructed a set of ate describing the relative vulnerability of female leopards candidate models based on alternative a priori hypotheses. to infanticide. Females were considered vulnerable if an We performed model selection using Akaike’s Information infanticide event occurred in an adjoining home range and Criterion (AIC) corrected for small sample size (Burnham if they had at least one dependent cub less than or equal to & Anderson 2002). We determined the maximum log likeli- six months old (76% of cubs killed through infanticide were hood for each candidate model and calculated the values for less than or equal to six months old; Table 5) or if they gave

AIC, delta AIC (DAICi = AICi - min. AIC, the minimum birth within three months of the event (assuming a gesta-

AIC value of all models) and the Akaike weight (wi, the tion period of 101 days; Skinner & Chimimba 2005). Demo- weight of evidence that model i is the best approximating graphic covariates used in models included maternal age, model given the set of candidate models considered). Where litter size and the number of cubs reaching independence. several models competed for the top rank (i.e. DAICi < 2), The identity of the mother was included as a random factor. we used multimodel inference to assess the relative strength We calculated all analyses and statistical computations of predictors (Burnham & Anderson 2002). We calculated using IBM SPSS 19.1 (SPSS Inc., Chicago, Illinois, USA). We the unconditional standard error and the 95% confidence tested all variables for normality and transformed data intervals of each covariate, and those variables whose where appropriate. Significance was measured at P < 0.05 standard error excluded zero were deemed significant and two tailed. We present means with standard errors as a (Mazerolle 2006). We used the variance inflation factor measure of precision. (cˆ = residual deviance/residual degrees of freedom) to test the data for overdispersion and Cook’s distances to identify RESULTS potential outliers (Mazerolle 2006). We limited our analyses on reproductive correlates to Reproductive parameters 2003–10 (n = 101 litters) as we had data on lion and leopard numbers in the SSGR for this period. Mean annual rainfall Female leopards began displaying signs of oestrus (scent was calculated for each year of the study. Rainfall might marking and calling; Wielebnowski & Brown 1998) at influence leopard reproduction through effects on vegeta- 26 Ϯ 2 months (n = 9, range = 18–36) and were first tive cover, which affect leopard hunting success (Balme et al. recorded mating at 35 Ϯ 3 months (n = 11, range = 24–46). 2007) and may affect the vulnerability of cubs to predation Mean age at first parturition was 46 Ϯ 2 months (Table 1), (Bailey 2005). It can also influence prey availability but we suggesting that females successfully conceived for the first found no correlation between impala Aepyceros melampus time at approximately 43 months. Age at primiparity was 2 numbers and mean annual rainfall in our study (Pear- not related to leopard abundance (R = 0.034, F1, 14 = 0.488, son’s correlation coefficient = 0.062, n = 8, P = 0.761). We P = 0.496). Mating pairs were typically observed associating included seasonality (either of birth or independence) as an for 2.4 Ϯ 0.2 days (n = 41, range = 1–7). The mean number additional covariate as it may have similar effects to rainfall of consortships observed between consecutive litters was (Laundré & Hernandez 2007). Impala comprised >50% of 2.8 Ϯ 0.5 (n = 72, range = 1–10), but the minimum number leopard diet in this area (Bailey 2005), so we used impala that must have occurred (including successful consortships population size throughout the SSGR (as determined by that were not observed) was 3.3 Ϯ 0.4. On average, female annual aerial censuses) as a proxy for relative prey abun- leopards mated with 1.3 Ϯ 0.1 males (range = 1–3) between dance (Sabi Sand Wildtuin, unpublished data). Each year, successive litters.

Fig. 2. Number of leopard litters recorded (bars) and mean rainfall (line; millimetre) in each month of the year in the Sabi Sand Game Reserve, South Africa, 1979–2010. The wet season spans October to March; the dry season spans April to September.

Leopards gave birth in all months of the year (n = 154 mean = 19 Ϯ 1 months, range = 9–31) and female cubs litters), but births were more frequent in the wet than in the (n = 38, mean = 18 Ϯ 1 months, range = 9–29; U = 746.500, 2 dry season (c 1 = 14.961, P < 0.001), and peaked in Decem- Z = 1.137, P = 0.255). Timing of litter independence was also ber (Fig. 2). The number of litters born per month was random; similar numbers of litters were left in the wet and 2 2 related to rainfall (R = 0.630, F1, 11 = 17.020, P = 0.002). dry seasons (c 1 = 0.380, P = 0.579). The likelihood of Thirty-one litters (22%) comprised a single cub, 95 litters (68%) comprised twins and 14 litters (10%) comprised triplets (Table 1). Our regression analyses suggested that the Table 2. A priori regression models and model averaged parameters best predictor of litter size was maternal age (Table 2). Litter predicting the effect of demographic and environmental factors on size appeared to remain relatively constant until females leopard litter size in the Sabi Sand Game Reserve, South Africa, 2003–10 were 13 years old and thereafter declined, although sample sizes for older age groups were relatively small (Fig. 3). Model no. Model set K† AICc‡ DAICc wi§ There was no difference in the size of primiparous (n = 32, 1 Maternal age 2 83.915 0 0.204 mean = 1.9 Ϯ 0.1, range = 1–2) and multiparous litters 2 Maternal age, leopard 3 84.477 0.562 0.154 (n = 108, mean = 1.9 Ϯ 0.6, range = 1–3; U = 1748.000, abundance P = 0.904). Although leopard and impala abundance were 3 Maternal age, impala 3 84.157 0.730 0.144 also included in models with DAIC < 2, their influence on abundance litter size was weak (Table 2). The ratio of male (n = 86) to Confidence interval 2 female cubs (n = 83) did not differ from parity (c 1 = 0.053, Parameter Estimate SE Lower Upper P = 0.818). Average age at independence of litters in our study area was Maternal age* 0.014 0.007 0.001 0.028 Leopard abundance 9.496 7.855 5.901 24.893 19 Ϯ 1 months (Table 1). Five models had DAIC < 2 but the - Impala abundance 7.426 7.335 -6.951 21.802 only variable exhibiting a strong effect was impala abundance (Table 3), which was negatively correlated with age at inde- *Parameter deemed significant as confidence interval excludes 0. 2 †The number of estimable parameters. pendence (Fig. 4; R = 0.161, F1, 51 = 9.612, P = 0.003). There ‡Akaike Information Criteria adjusted for small sample sizes. was no difference in the age that mothers abandoned litters §Akaike weight. Ϯ with single cubs (n = 33, mean = 19 1 months, range = 9– Explanations of the predictors included are provided in the text. Only Ϯ 31) and two cubs (n = 19, mean = 18 1 months, range = 9– candidate models with DAICc < 2 are shown. 25; U = 293.000, Z =-0.391, P = 0.696), or male (n = 34, SE, standard error.

Fig. 3. Mean litter size (line) recorded for female leopards aged 3–15 years in the Sabi Sand Game Reserve, South Africa, 1979–2010. Bars represent standard errors; numbers above bars denote the sample sizes for the means (number of litters recorded for each maternal age class).

recruitment into the adult breeding population did not generally gave birth 6 Ϯ 1 months (n = 37, range = 1–19) appear to be inﬂuenced by age at independence (recruited: after their previous litter became independent or 8 Ϯ 1 n = 31, mean = 18 Ϯ 1 months, range = 9–26; not recruited: months (n = 46, range = 2–22) after a litter was lost (although n = 9, mean = 17 Ϯ 2 months, range = 9–29; U = 152.500, females resumed mating from 12 days after losing a litter). No Z = 0.424, P = 0.679). female cared for more than one litter simultaneously, but at The interval between births of successive litters differed least 41% were pregnant when accompanied by old cubs. when at least one cub survived to independence and when no cubs survived to independence (Table 1, U = 2383.000, Cub survival Z = 7.631, P < 0.001). Similarly, the time taken by females to replace litters differed for successful and unsuccessful Only 47% of known cubs (n = 251, we censored eight cubs litters (U = 580.500, Z =-2.489, P = 0.013). Female leopards that were still alive at the end of the study) survived to inde-

Table 3. A priori regression models and Model no. Model set K AICc DAICc wi model averaged parameters predicting the effect of demographic and environmental 1 Maternal age, impala abundance 3 304.554 0 0.245 factors on the age at independence of leopard 2 Maternal age, impala abundance, annual rainfall 4 304.753 0.199 0.222 litters in the Sabi Sand Game Reserve, South 3 Impala abundance 2 305.492 0.938 0.153 Africa, 2003–10 4 Impala abundance, annual rainfall 3 306.136 1.582 0.111 5 Maternal age, impala abundance, seasonality 4 306.519 1.965 0.092

Conﬁdence interval

Parameter Estimate SE Lower Upper

Maternal age 0.001 0.001 -0.001 0.003 Impala abundance* -1.354 0.412 -2.160 -0.547 Annual rainfall 0.342 0.244 -0.135 0.820 Seasonality 0.050 0.067 -0.081 0.181

*Parameter deemed signiﬁcant as conﬁdence interval excludes 0. Explanations of the predictors included are provided in the text. Only candidate models with

DAICc < 2 are shown. Abbreviations as in Table 2.

Fig. 4. Relationship between the estimated abundance of impala Aepyceros melampus (the main prey of leopards) and age at independence of litters for leopards in the Sabi Sand Game Reserve, South Africa, 1979–2010 2 (R = 0.161, F1, 51 = 9.612, P = 0.003). pendence. If we include estimates for litters that disap- abandoned by its mother, but it was adopted by another peared before cubs were counted (n = 33), survivorship to female leopard (its grandmother) and survived to indepen- independence dropped to 37%. Cumulative cub survival dence (Balme et al. 2012a). African rock pythons Python declined rapidly with age (Fig. 5a). Only 55% of cubs sur- sebae preyed on three cubs in their dens, and a 12-month- vived their first three months, 44% survived to six months, old cub died after being bitten by a Mozambique spitting 40% to nine months, 38% to 12 months and 37% survived cobra Naja mossambica. Two litters (aged two months) to 18 months. There was no difference in survival of male drowned in their dens during heavy storms. Except for a 2 and female cubs (c 1 = 0.319, P = 0.572) or of cubs born in six-month-old female that contracted and died from 2 the wet and dry seasons (c 1 = 2.867, P = 0.090). Litter sur- mange, disease was not recorded as a mortality factor of vival showed a similar trend to cub survival; at least one cub cubs. The likelihood of at least one cub in a litter surviving survived to independence in only 49% of litters (n = 166, six a mortality event increased significantly with age (Table 6; litters censored), and most mortality occurred in the first Spearman’s rho =-0.507, P < 0.001). three months (Fig. 5b). Our logistic regression models suggested that exposure to infanticide and maternal age were Reproductive success the only significant factors affecting litter success (Table 4). Cub survival declined once females were 9 years old and Female leopard survival was lowest in the first year, contin- then dropped rapidly after 14 years (Fig. 6). ued to decline until 7 years, stabilized temporarily and then We were able to determine the cause of death for 98 cubs decreased again after 16 years (Fig. 7). The oldest known- (Table 5). Infanticide accounted for most mortality, fol- age female was 18.6 years. The oldest female we recorded lowed by predation by lions and spotted hyaenas. Only giving birth was 16.3 years. The highest number of litters male leopards were recorded committing infanticide. Cubs documented for a single female was 11, comprising 19 cubs, killed by lions and leopards were a similar age, but those of which four survived to independence. After females 2 killed by hyaenas tended to be younger (c 2 = 11.632, reached sexual maturity, maternity rates remained relatively P = 0.003). Two cubs, aged four and six months, presum- constant throughout their lives (with peaks at 4, 6, 8 and 11 ably starved when their mothers died, as did a three- years corresponding to a 25-month interbirth interval), only month-old cub that was separated from its family by a decreasing notably at 16 years old (Fig. 8). Maximum per flooding river. Only one other cub (aged six months) was capita cub production occurred at 8 years.

Fig. 5. Cumulative survival of leopard (a) cubs and (b) litters in the Sabi Sand Game Reserve, South Africa, 1979–2010. Successful litters were those in which at least one cub survived to independence.

We documented complete reproductive histories for 15 were both negatively correlated to cub survival and to each female leopards that had at least one cub survive to inde- other. LRS was negatively related to the proportional pendence. The average LRS for females was 4.1 Ϯ 0.8 number of female cubs raised to independence (R2 = 0.474,

(Table 7a). Although all three life history traits made sub- F1,14 = 11.708, P = 0.005). stantial contributions to LRS, cub survival appeared the most important, accounting for 62% of the variance if DISCUSSION longevity and fecundity were set equal to their means (Table 7b). Percentage contributions of all three traits Our study is the ﬁrst to examine comprehensively the envi- totalled more than 100 because longevity and fecundity ronmental and demographic factors affecting leopard

Table 4. A priori regression models and Model no. Model set K AICc DAICc wi model averaged parameters predicting the 1 Maternal age, exposure to infanticide, lion 4 119.438 0 0.531 effect of demographic and environmental abundance factors on leopard litter success (i.e. the 2 Maternal age, exposure to infanticide, impala 8 120.065 0.627 0.388 likelihood that at least one cub in a litter abundance, lion abundance, litter size, survived to independence) in the Sabi Sand annual rainfall, seasonality Game Reserve, South Africa, 2003–10

Conﬁdence interval

Parameter Estimate SE Lower Upper

Maternal age* -0.092 0.036 -0.162 -0.022 Exposure to infanticide* -2.293 0.552 -3.375 -1.212 Impala abundance -0.709 1.776 -4.190 2.772 Lion abundance 12.603 7.088 -1.289 26.495 Litter size -0.963 0.535 -2.012 0.086 Annual rainfall 9.773 7.312 -4.559 24.105 Seasonality -0.765 0.537 -1.818 0.288

*Parameter deemed signiﬁcant as conﬁdence interval excludes 0. Explanations of the predictors included are provided in the text. Only candidate models with

DAICc < 2 are shown. Abbreviations as in Table 2. reproduction in a stable, protected population. It therefore in leopard births in the adjoining Kruger National Park and represents a baseline for comparison with future research suggested that females synchronized births to take advan- and to inform management decisions pertaining to the tage of impala lambs born at a similar time. Lactation is the species. most energy demanding part of the reproductive cycle, since mothers must maintain themselves as well as produce milk for their offspring (Bronson 1989). Females must also Reproductive parameters restrict their movements around den sites while nursing Leopards in the SSGR appeared to exhibit a birth pulse; the young cubs. Hence, timing births when food is predictably majority of litters were born during the wet season, particu- abundant and vulnerable should be an adaptive strategy larly in December. Bailey (2005) documented a similar peak that enhances cub survival (Logan & Sweanor 2001).

Fig. 6. Mean proportion of cubs surviving to independence (line), produced by female leopards aged 3–16 years in the Sabi Sand Game Reserve, South Africa, 1979–2010. Bars represent standard errors; numbers above bars denote the sample sizes for the means (total number of cubs recorded for each maternal age class).

Table 5. Causes of mortality, proportions of No. of Proportion of Age of cub at litters lost and mean ages at death for leopard deaths litter lost death (months) cubs in the Sabi Sand Game Reserve, South Africa, 1979–2010 Cause of mortality N % Mean SE Mean SE Min Max

Infanticide 39 40 0.7 0.1 5 1 1 15 Lion 27 28 0.7 0.1 4 1 1 18 Spotted hyaena 14 14 0.6 0.1 2 0 1 5 Abandoned 4 4 0.7 0.3 5 1 3 7 Drowned 4 4 1.0 0 2 0 2 2 Snake 4 4 0.8 0.2 4 3 1 12 Banded mongoose Mungos mungo 2 2 1.0 0 1 0 1 1 Nile crocodile Crocodylus niloticus 1 1 0.3 – 9 – – – Martial eagle Polemaetus bellicosus 1 1 0.5 – 3 – – – Honey badger Mellivora capensis 1 1 0.5 – 2 – – – Disease – mange 1 1 1.0 – 6 – – –

Min, minimum; Max, maximum; SE, standard error.

However, we detected no difference in survival rates among males. Such behaviour has been documented in several leopard cubs born in the wet and dry seasons. Habitat mammalian species where subadult females remain in modification and the creation of numerous artificial water contact with male relatives (Pusey & Wolf 1996, O’Riain sources in the SSGR during the last 30 years have reduced et al. 2000). Mean male leopard tenure in our study area was seasonal fluctuations in impala numbers, resulting in a 4.6 Ϯ 0.6 years (Balme et al., in prep.); hence, there was stable year-round prey base for leopards (Owen-Smith & considerable opportunity for sexually mature daughters to Ogutu 2003). Therefore, the benefits of seasonal breeding in mate with their fathers. However, such incidents comprised our study area were probably diminished, but insufficient only 5% of observed consortships and levels of inbreeding time may have elapsed for female leopards to adapt to the appeared low (mean coefficient of relatedness between con- altered conditions. sorting pairs = 0.04 Ϯ 0.01; Balme et al., in prep.). Mean age Primiparity among female leopards appears to be influ- at first parturition was older in our study (46 months) than enced by social as well as physiological factors. Females in recorded for two lower density leopard populations in our study were first recorded mating at approximately 3 South Africa (Karongwe Game Reserve: 37 months, Owen years old. At this age, they are still in the process of et al. 2010; Phinda Game Reserve: 40 months, Balme 2009). establishing territories and, although physiologically Intraspecific competition is generally less intense at low capable of conceiving, it is unlikely that they could success- population densities, which may allow females to establish fully raise cubs until settled (Bailey 2005). Most females territories earlier and give birth when younger (Festa- have established residency by 4 years, securing access to Bianchet et al. 1998). the resources necessary for pregnancy, lactation and cub Mean litter size observed in our study (1.9) was slightly rearing. Delayed primiparity may also have evolved as an larger than reported elsewhere (Serengeti National Park, inbreeding avoidance mechanism. Philopatric female leop- Tanzania: 1.4, Schaller 1972; Kgalagadi Transfrontier Park, ards may have postponed reproduction until their fathers South Africa: 1.5, Bothma & le Riche 1984; Chitwan were ousted from their territories and replaced by unrelated National Park, Nepal: 1.7, Seidensticker et al. 1990; Karongwe Game Reserve: 1.6, Owen et al. 2010; Phinda Game Reserve: 1.6, Balme 2009). This may be a reflection of the earlier age that cubs were first encountered in our study, Table 6. Age-specific likelihood of an entire leopard litter being lost assuming high levels of pre-emergent cub mortality. None- during a mortality event in the Sabi Sand Game Reserve, South Africa, theless, our median litter size of two concurred with that of 1979–2010 other studies. The energetic costs involved in producing No. of Probability of large litters may have been excessive for old female leopards, Age mortality No. of whole-litter possibly explaining the decrease in litter size after 13 years. (months) events litters lost loss (%) Lions in Serengeti National Park show a similar drop in 0–2 64 50 78 litter size at the same age (Packer et al. 1998). Unlike in 2–4 36 15 42 many other carnivore species (Tannerfeldt & Angerbjörn 4–6 11 3 27 1998, McDonald & Fuller 2001), litter size in leopards was >61119not related to prey abundance. Management intervention in Total 122 69 57 the SSGR ensured that impala numbers were artificially

Fig. 7. Cumulative survival of female leopards in the Sabi Sand Game Reserve, South Africa, 1979–2010. high and, even during lean periods, it is unlikely that the independent youngsters; however, cubs that stayed with leopard population was resource limited. However, very their mothers for longer did not appear any more likely to large sample sizes are required to assess the demographic be recruited into the breeding population. Even though and environmental determinants of litter size accurately females spent a small proportion of their time with cubs of because there is limited variation in the number of young over one year old, associating mainly at kills, they gave birth born to carnivores (Schwartz et al. 2006). again only once their previous litter was independent. No There was considerable variation in the age that cubs female in our study cared for more than one litter concur- became independent. We could not determine the fate of all rently (although this has been reported anecdotally from

Fig. 8. Mean numbers of cubs produced per year (line) by female leopards aged 3–18 years in the Sabi Sand Game Reserve, South Africa, 1979–2010. Bars represent standard errors; numbers above bars denote the sample size for the means (total number of breeding and non-breeding females in each age class).

Table 7a. Means and variances of individual components of lifetime and when they are ﬁrst led to kills by their mothers (Le reproductive success and their products for female leopards in the Roux & Skinner 1989). Dens are focal points of activity as Sabi Sand Game Reserve, South Africa, 1979–2010 females move back and forth between hunting and nursing. Component Mean Variance Such activity is likely to generate visual, auditory and olfac-

Longevity 9.3 23.2 tory cues that increase the chances of predation. The relative Fecundity 1.36 0.4 immobility of young cubs and their inability to climb trees Cub survival 0.4 0.1 until two months old (GA Balme, pers. obs.) also increases Longevity ¥ cub survival 10.8 37.5 their vulnerability, as evidenced by the high proportion of Longevity ¥ fecundity 3.8 7.0 litters lost at this age. Fecundity ¥ cub survival 0.4 0.1 Infanticide was the most common source of cub mortal- Lifetime reproductive success 4.1 10.1 ity, accounting for 40% of known-cause deaths. Our multivariate analysis similarly showed that exposure to infanticide was a key determinant of litter success. Although Table 7b. Percentage contribution of individual components of there are several hypotheses explaining why infanticide lifetime reproductive success (LRS) to variation in LRS for female evolved (e.g. nutritional gain, competitive exclusion, paren- leopards in the Sabi Sand Game Reserve, South Africa, 1979–2010 tal manipulation of progeny and sociopathology; see Hrdy (see Brown 1988) 1979 for review), sexual selection appears the primary Component Longevity Fecundity Cub survival driver for the behaviour in leopards. On most occasions, Longevity 45 infanticide was committed by incoming (assumedly unre- Fecundity -33 42 lated) males that later established home ranges overlapping Cub survival -27 -54 62 those of affected females. A transient individual (a male leopard that subsequently left the area without breeding) was responsible for only one of the 27 incidents of infanti- other areas; Scott & Scott 2003, V. Athreya, pers. comm.). cide where the perpetrator was identified. Most attacks, par- Therefore, females that left cubs earlier were likely to ticularly those involving cubs less than four months old, produce more litters and have higher LRS. However, our resulted in the complete loss of litters. This prompted results suggest that increased fecundity must be balanced females to return to oestrus and shortened the interval with food availability. Given their relative inexperience, it between litters (although actual replacement time was seems likely that the survival of newly independent cubs longer). Infanticide was therefore likely to improve the increases with prey abundance. Mothers may therefore be fitness of male leopards by accelerating their opportunity to more inclined to leave cubs during prey-rich periods. More- father offspring, which extended their reproductive life over, increased food supply may accelerate growth and spans (Packer et al. 1988). shorten time to maturation (Owen et al. 2010). Mean age at Female leopards appear to adopt several strategies to independence in our study (19 months) was older than that counter the threat of infanticide. Our observations showed recorded in Karongwe Game Reserve (12 months; Owen that females often courted multiple males between the et al. 2010) and Phinda Game Reserve (13 months; Balme births of successive litters. Polyandrous mating has been 2009). Although prey abundance in these areas was compa- documented in several carnivore and primate species and is rable to SSGR, leopard population density was lower, which thought to be a mechanism employed by females to increase should result in higher per capita food availability. paternity uncertainty (Wolff & Macdonald 2004). Cub survival may be enhanced in such cases, as males should be less inclined to kill cubs that they may have sired. In addition to Cub survival increased promiscuity, female lions display a period of Although there are few reliable data for comparison, cub reduced fertility immediately following the takeover of a survival in our study (37%) was lower than previously pride by a new male coalition (Packer & Pusey 1983). This documented for the species (Kruger National Park: 50%, potentially allows lionesses to assess the fitness of new males Bailey 2005; Phinda Game Reserve: 58%, Balme 2009; and postpone conception until the threat of further take- Karongwe Game Reserve: 53%, Owen et al. 2010). Again, overs has diminished. We do not have conclusive data for this may be a result of litter size being underestimated leopards in the SSGR, but the time taken for females to in other studies. Even our estimates of survivorship were replace litters lost to infanticide was longer than the time conservative, as some cubs or even whole litters may have following successful litters, even though females were died undetected. Leopard cubs were most vulnerable during recorded mating soon after losing cubs. Balme et al. (2009) their first four months. This spans the time that cubs are showed that leopard mating success (defined as the number confined to dens (usually for six to eight weeks after birth) of litters produced per mating bout observed) in Phinda

Game Reserve was lower during a period of high male turn- tions (Packer et al. 1998, Schwartz et al. 2003). It occurred over than during a more stable period. Although female late in life, the number of individuals surviving to this age leopards in our study typically attempted to defend their was small and their overall contribution to recruitment was cubs from incoming males, they were almost always unsuc- minimal. cessful. Solitary carnivores appear more susceptible to The LRS of leopards (4.1 Ϯ 10.1) was comparable to that infanticide than social species simply because they cannot of other large felids (lion: 3.8 Ϯ 7.8, Packer et al. 1988; rely on cooperative defence (Packer et al. 2009). cheetah: 3.5 Ϯ 4.9, Kelly et al. 1998; tiger: 4.5 Ϯ 11.5, Smith Our analyses showed that cub survival was also influ- & McDougal 1991). When we partitioned LRS into its sepa- enced by maternal age. Intuitively, older female leopards rate components, variation in cub survival was the most should be better mothers, and reproductive success has been important contributor to variation in LRS. We presumably positively linked to experience in cheetahs (Pettorelli & underestimated the importance of cub survival because we Durant 2007). However, cub survival in our study decreased defined reproductive success as the number of individuals once females reached 9 years old and dropped notably reaching independence when it should be the number of after 14 years. Dispersal in leopards is generally sex biased; cubs recruited into the breeding population (Clutton-Brock females are philopatric and males disperse long distances 1988). Several studies have shown that offspring survival from their natal area (Bailey 2005). As with other carnivores after independence can have a significant effect on variation that form matrilineal assemblages (Logan & Sweanor 2001, in LRS (Clutton-Brock et al. 1988, Fitzpatrick & Wool- Goodrich et al. 2010), female leopards often relinquish parts fenden 1988). This suggests that parental care extends of their home range to establishing daughters (Fattebert beyond the weaning period, which in female leopards is et al., in prep.). Consequently, the home ranges of females likely to be manifested through the kin-related spatial that raise several daughters to independence should con- structure of females (Støen et al. 2005). Cub survival was tract as they get older, potentially to the point where inversely related to fecundity because females that lost their resource limitation impacts cub survival. Unfortunately, we cubs resumed breeding more rapidly than those that suc- do not have sufficient long-term spatial data to demonstrate cessfully raised litters to independence. Cub survival and such range contraction; however, LRS was lower for reproductive longevity were also negatively correlated, pre- mothers that raised proportionally more female cubs to sumably reflecting the inferior reproductive performance of independence. Since male leopards usually disperse, they are older female leopards. The negative relationship between unlikely to affect their mother’s access to resources and con- fecundity and longevity may be a statistical artefact that sequently her ability to raise cubs. This seemingly altruistic arose from excluding non-breeders (Packer et al. 1988). behaviour by female leopards presents a possible illustration Individuals that died soon after maturity had dispropor- of kin selection, where an individual enhances its inclusive tionately high fecundity because of their relatively short fitness by assisting a relative, even though its own reproduc- life spans. tion may suffer as a result (Hamilton 1964). CONCLUSION Reproductive success Our results suggest that the reproductive success of female Maternity rates for leopards mirrored the classic bell-shaped leopards in the SSGR is regulated primarily by top-down productivity curve evident in many carnivore species processes. Offspring survival was the most important vari- (Schwartz et al. 2003). Cub production increased rapidly able affecting LRS, and predation (predominantly by male during sexual maturity, reached a peak between 8 and 11 leopards, lions and spotted hyaenas) accounted for 91% of years and declined gradually thereafter, only dropping off at cub mortality. Similarly, our logistic regression models 16 years. Females suffered increased mortality from 3 to 7 showed that exposure to infanticide was a key factor deter- years presumably while they secured their newly established mining the likelihood of a female successfully raising cubs territories (Bailey 2005). This may explain why cub produc- to independence. This has significant management implica- tion only peaked at 8 years even though most females began tions. The leopard population in the SSGR appeared breeding at 4 years old. Reproductive senescence approxi- capable of withstanding the high incidence of infanticide mated physical longevity in our study. It is possible that old observed in our study (the population remained relatively females had lower fertility, as cub survival among this age stable throughout the study period); however, activities such class was lower than for prime-aged females; however, as trophy hunting that artificially elevate turnover among shorter interbirth intervals and correspondingly higher breeding males may increase rates of infanticide to unsus- fecundity would then be expected but did not occur. Even tainable levels (Whitman et al. 2004, Packer et al. 2009). It so, it seems unlikely that reproductive senescence would seems unlikely that cub survival would adjust through some have much effect on the intrinsic growth of leopard popula- compensatory response; infanticide was not related to

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