REPRODUCTIVE PARAMETERS OF WILD FEMALE AMUR (SIBERIAN) TIGERS (PANTHERA TIGRIS ALTAICA)
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1 Journal of Mammalogy, 8():88 98, REPRODUCTIVE PARAMETERS OF WILD FEMALE AMUR (SIBERIAN) TIGERS (PANTHERA TIGRIS ALTAICA) LINDA L. KERLEY, JOHN M. GOODRICH,* DALE G. MIQUELLE, EVGENY N. SMIRNOV, HOWARD B. QUIGLEY, AND MAURICE G. HORNOCKER Hornocker Wildlife Institute and Wildlife Conservation Society, Stadium Drive, Suite a, Bozeman, MT 5979, USA (LLK, JMG, DGM, HBQ, MGH) Sikhote-Alin State Biosphere Zapovednik, Terney, Primorye Krai 695, Russia (ENS) We monitored reproduction of female tigers (Panthera tigris altaica) on and near the Sikhote-Alin Biosphere Zapovednik, Russia, 99, using radiotelemetry, capture, and conventional tracking (using snow and soil substrates). Tigers gave birth in all but months of the year, with a peak in late summer (.68, d.f., P.; n 9 litters from mothers). Minimum age of st reproduction for tigers was. years (mean 95% confidence interval). Mean interval between litters was.. months (n 7 pairs of consecutive litters for tigers). Mean litter size was..6 cubs (n 6 litters of 9 tigers) when litter size was st determined but, due to 7% cub mortality (n 9 litters), decreased to..5 cubs (range, n 9 litters) by the time cubs were months old. At least 57% of cub mortality was anthropogenic. Mean age at dispersal was months (n 5 litters). Mean reproductive rate was. cubs/year, but only.7 cubs/year survived up to months old. We believe that recent conclusions that tiger populations can grow and recover rapidly from substantial losses may be overly optimistic. Key words: Zapovednik (Siberian) tiger, cubs, dispersal, Panthera tigris altaica, litter size, reproduction, Tigers (Panthera tigris) are endangered throughout their range (Mills and Jackson 99; Nowell and Jackson 996; Seidensticker 986; William and Rabinowitz 996), and understanding their reproductive parameters is critical for developing sound conservation strategies. For example, an understanding of reproduction and recruitment rates is needed to estimate what human-induced mortality rates a population can sustain (Ahearn et al. ; Kenney et al. 995; Smirnov and Miquelle 999), to examine metapopulation dynamics (e.g., determining the reproductive output of source populations), and for population modeling and estimating minimum viable population size (Smith and McDougal 99). Yet, reproductive parameters of wild * Correspondent: tiger7@yahoo.com tiger populations are poorly known. The majority of information comes from captive animals (Kleiman 97; Sadleir 966; Seal et al. 987) and wild population of Bengal tigers (P. t. tigris McDougal 977; Smith and McDougal 99; Sunquist 98). Because tigers are widely distributed across Asia (Nowell and Jackson 996; Wikramanayake et al. 999), reproductive parameters may vary between the 5 extant subspecies in response to different climates, habitats, prey densities, and other environmental parameters. Information on how reproductive parameters vary between different areas and subspecies is essential for range-wide conservation planning. The tiger (P. t. altaica), the northernmost subspecies, is faced with harsh environmental conditions including severe winters and low prey densities (Miquelle et 88 Downloaded from on August 8
2 February KERLEY ET AL. REPRODUCTION AND AMUR TIGERS 89 al. 999b). Current information on reproductive parameters of tigers is based on snow tracking (Abramov V. K. 96; Abramov K. G. 977; Baikov 95; Bragin 989; Matyushkin 98; Matyushkin et al. 999; Salkina 99; Smirnov 986; Smirnov and Miquelle 999; Yudakov and Nikolaev 987), which has limited applications because individuals cannot be positively identified or monitored over extended or snowfree periods. We analyzed data collected during a 9-year period on and near the Sikhote- Alin Biosphere Zapovednik in the Russian Far East, using a combination of radiotelemetry, live capture, and conventional tracking, to describe reproductive parameters of tigers in the wild. We compare our findings with existing information on tigers (much in Russian sources) and Bengal tigers in Nepal, where prey densities are much higher and tiger home-range sizes much smaller than those in the Russian Far East (Goodrich et al. 999; Miquelle et al. 999a; Smith et al. 987). MATERIALS AND METHODS We studied reproductive activities of tigers on and near the 9,8-ha Sikhote-Alin Biosphere Zapovednik (hereafter, Zapovednik) in Primorye Province, Russia ( 6 N, 5 8 E). Russian Zapovedniks (state reserves) are highly protected lands with minimal human disturbance; access is restricted to scientists and forest guards (Stepenitski 996). The eastern border of the reserve is the coast of the Sea of Japan, and its central feature is the Sikhote-Alin Mountain Range, which parallels the coastline. Elevations range from m to nearly,6 m, but most mountain peaks are below, m. Secondary Mongolian oak (Quercus mongolica) forests are common near the coast and a mixture of Korean pine (Pinus koraensis), larch (Larix komarovii), birches (Betula costata, B. lanata, and others), basswood (Tilia amurensis), and Khingan fir (Abies nephrolepis) persists more inland and at higher elevations. The land surrounding the Zapovednik includes a 7,5-ha buffer zone ( 8 km wide) where human activities include fishing, hunting, tourism, and some agricultural practices such as livestock grazing and hay cutting. More descriptions of the region and environmental variables potentially influencing tiger reproduction can be found elsewhere (Knystautas and Flint 987; Miquelle and Smirnov 999; Miquelle et al. 996, 999a, 999b; Newell and Wilson 996). We monitored reproductive activities of adult female tigers from January 99 through December ; 9 were radiocollared, and were monitored by tracking litter each of radiocollared cubs (Table ). We captured and fitted tigers with radiocollars using methods described in Goodrich et al. (). Each animal was assigned a letter designating sex (F female and M male) and a unique number. We monitored and recorded locations of radiocollared tigers from the ground (on foot and from vehicles) and from the air in a biplane (Antonov- ) or helicopter (MI-8). Ground locations were obtained by triangulation, approaching within m and partially circling the tiger, visual observations, and subsequently locating tracks (especially in snow, but also in various soil substrates) in an area where we detected a tiger s radiosignal. In using track data (in snow or soil), we did not attempt to identify individuals based on specific track characteristics (Das and Sanyai 995; Karanth 987) but compared track measurements (particularly pad width) found in the field to known measurements of captured females to verify location, presence or absence of litter, and litter size of females. General estimates of track size were used to identify adult males, females, and cubs following Smirnov and Miquelle (999) and Matyushkin et al. (999). Reproductive parameters. We estimated the following reproductive parameters: age at st reproduction, seasonality of conception and birth, length of gestation, mean interval between litters (when the st litter in a pair of consecutive litters survived at least months), mean litter size, cub mortality, sex ratio of litters, and cub age at dispersal (when cubs left their natal home ranges). We used the following age categories: cubs (associated with and dependent on their mothers), subadults (no longer associating with their mothers but not yet having reproduced), and adults (having reproduced at least once). We estimated ages by comparing tooth wear (Ashman et al. 98), body weight, and body and track measurements (Nikolaev and Yudin 99) and by behavioral observation, i.e., young tigers traveling with their mothers (cubs), scent marking and other territorial behaviors (associated with Downloaded from on August 8
3 9 JOURNAL OF MAMMALOGY Vol. 8, No. TABLE. Reproductive histories of female tigers radiotracked from January 99 to December on and near the Sikhote-Alin Biosphere Reserve in Russia, as part of the Siberian Tiger Project. Female no. Time monitored (months) Captured as adults 5 7 a b. Captured as cubs or subadults Time to st litter after being radiocollared (months). Captured with two -month-old cubs 7.. Captured two -month-old cubs Never reproduced Never reproduced Never reproduced Never reproduced Number of litters during monitoring period Status as of December Presumed dead Unknown Alive Alive Alive Alive Unknown, transmitter failure Dispersed, unknown a Female no. 7 was never radiocollared, but her litter was monitored by tracking her radiocollared offspring. b Calculated from time of captures to time when cubs were at least months old (after which cubs were rarely with their mother). adults or newly established subadults Smith et al. 989), or females traveling with cubs (adults). We estimated minimum age of st reproduction for all females monitored from years of age until their death or disappearance, assuming that successful reproduction does not occur before years of age (Christie and Walter ; Smith 98). We estimated birth dates of litters by or a combination of the following indicators: females usually localized their movements just before and up to months after the birth of a litter (Smith and McDougal 99); extrapolation of birth dates from observations and radiolocations of female male pairings and indications of mating behavior, e.g., roaring (Smith and McDougal 99); by tooth replacement patterns of young (canines are replaced at approximately months Mazak 98); and by estimating cub ages based on body size (when captured or observed) and track size (as above). We include an estimate of error for each birth date based on an assessment of accuracy (day of localization for denning may have an error of 7 days, depending on frequency of locations, but for estimates of tooth replacement we considered error to be month). Recognizing the potential errors in our age estimates, we looked for seasonality in birth dates at a gross scale by comparing the number of litters born in each of seasons, early winter (November January), late winter (February April), early summer (May July), and late summer (August October), using a chi-square test for equal proportions (SAS Institute Inc. 996). Because of small sample sizes, we selected these seasons post hoc to maximize the probability of detecting a difference. We estimated length of gestation for female whose pairing with a male and birth date were well defined. We estimated month of conception for other females from known birth dates by assuming that gestation lasts, on average, for days (Kitchener 99; review in Nowell and Jackson 996; Sankhala 978). We determined litter sizes, sex ratio, cub mortality and survival by visual observation, radiolocations of cubs themselves, or, more often, by the presence or absence of cub tracks (especially in snow) in association with a radiocollared tigress. If cubs were not sexed by direct observations, we determined their sex using track measurements at about year of age, when Downloaded from on August 8
4 February KERLEY ET AL. REPRODUCTION AND AMUR TIGERS 9 males are % larger than females (Smith and McDougal 99), tracks of male cubs (pad width cm) are generally larger than tracks of adult females (pad width generally cm), and tracks of female cubs are still smaller than adult females (pad width generally 9 cm Smirnov et al. 999; Yudakov and Nikolaev 987). Because the sex of most cubs was determined using track measurements at months, our estimation of litter sex ratio likely does not represent sex ratio at birth. If cubs were not radiocollared but we found their tracks with those of their mothers at or beyond months of age, we assumed that they survived and were recruited into the population; if we lost their tracks before months of age, we assumed they died. If action was taken to prevent the death of cubs after the death of their mother (i.e., removal from the wild or supplemental feeding in the wild), we assumed these cubs would have died without those actions and included them in our estimates of mortality. To include all litters for calculating cub mortality rates, for those litters whose size was unconfirmed in the first months, we used values for litter size: we assumed litter size to be the minimum (i.e., ) or we assumed litter size was the average for all others at st detection. We calculated age of dispersal for radiocollared cubs that dispersed as the age at which we st located each cub 5 km from the boundary of their mothers home range. We estimated reproductive rate of female tigers using mean litter size/mean birth interval (J. J. Craighead et al., in litt.; Wielgus and Bunnell 99), total lifetime productivity (total number of cubs produced in a lifetime Sunquist 98), and total lifetime reproduction of young surviving their st year. This last value is slightly different from that estimated by Smith and McDougal (99) of lifetime reproduction of dispersal young, but it provides a basis for comparison. In estimating total lifetime productivity, we assumed that females are reproductively active until years of age (Crandall 96; Kleiman 97; review in Nowell and Jackson 996): the oldest known-age tigress was in Nepal and was killed when she was at least 5.5 years old (McDougal 99). Data are reported as mean SD. RESULTS FIG.. Times of birth and conception for tiger litters on and near the Sikhote-Alin Biosphere Zapovednik in Russia, 99. Conception dates were birth dates minus estimated gestation period ( days). We estimated minimum age of st reproduction as. years (mean 95% confidence interval) based on observations of female tigers: female produced her st litter at.5 years of age ( month); female at.5 years of age ( year); female had still not reproduced at years of age (.5 months) when her collar failed; and female 7 had not yet reproduced at years of age ( 6 months) when she was killed by poachers. We consider our estimate a minimum age of st reproduction because of the animals had not yet reproduced at years of age. Our assumption that reproduction does not occur before years of age was supported by additional observations: female 5 had not yet reproduced at years of age when she was killed by poachers, and female 6 dispersed and we lost her signal at months of age, before she reproduced. Tigers gave birth in all but months of the year (n 9 litters from mothers; Fig. ), but births were most frequent in late summer (.68, d.f., P.). Based on these estimates of birth dates, corresponding conceptions were most frequent from March to May (Fig. ). Because litters were detected at different ages and by using different methods, error in estimating litter birth dates varied from to days (Table ). The gestation period of female tiger (female 5) with well-defined conception Downloaded from on August 8
5 9 JOURNAL OF MAMMALOGY Vol. 8, No. TABLE. Litter characteristics of female tigers that reproduced and were monitored between January 99 and December on and near the Sikhote-Alin Biosphere Zapovednik, Russia. Female no. Mother of no. a Litter no. 5 7 a 5 7 Litter birth date ( days) Feb. 99 ( ) 7 Jul. 99 ( ) Oct. 995 ( ) 5 Oct. 997 ( ) Litter birth interval (month days) 8 Aug. 99 ( ) Sep. 99 ( 5) Aug. 996 ( ) 5 Oct. 998 ( ) 8 Oct. 99 ( ) 7 Aug. 99 ( 7) Aug. 995 ( 7) Apr. 995 ( ) Dec. 995 ( 7) Jul. 997 ( 7) 7 May 99 ( ) 5 Jun. 998 ( ) Aug. 999 ( 7) 5 May ( ) Jun. ( ) Cub age (months) when litter size determined NA c NA NA Litter size Unk d Unk e Unk e a Litters were monitored by tracking radiocollared cubs. b Unk indicates unknown. c NA, not available. d An unknown number of cubs were presumed dead after their mother was poached. Litter size at months Causes of mortality within litter Unk b Shot, unk Mother poached Predation, unk Unk Natural, possibly predation Mother poached Mother poached and birth dates was between and 8 days. This female (female 5) also gave birth 7 months after she lost her -week-old litter to unknown causes. For females whose litter survived at least months, the mean interval until the next litter was.. months (range 6 months, n 7 pairs of consecutive litters born to tigers; Table ). Females had shorter birth intervals after raising single cubs (5.5.9 months, n intervals and tigers) than after raising cub (.8. months, n 5 intervals and tigers; t.9, d.f., P.9). On average, we st determined litter size when cubs were.9.6 months old (n 6); nearly 7% of the litters were months old when litter size was st detected. Mean litter size was..6 cubs/ litter (range cubs, median.5 cubs, mode cub, n 6 litters of 9 females; Table ) when litter size was st determined but decreased to..5 cubs/ litter (range cubs) by the time litters were months old. Cub mortality was 7% during the period from st detection to months of age, the range depending on our methods, i.e., whether litters of unknown size were allocated initial sizes of (minimum) or. (mean; n 9 litters and cubs). Sex ratio of litters when cub sex was st detected was female biased (.5.9 females/male cub, n litters); litters of single cubs were all females. Cubs died, or were removed from the wild and therefore considered mortalities in our analysis, from several causes (Table ). Two cubs representing litters died of natural causes at month of age ( was killed by a small predator and died of Downloaded from on August 8
6 February KERLEY ET AL. REPRODUCTION AND AMUR TIGERS 9 unknown but nonanthropogenic causes at week of age), 6 cubs from 6 litters (including complete litters of unknown sizes) died of unknown causes, and 9 cubs from litters (5% of total cub mortality, n 7 dead cubs) died, or would have died without our intervention, because of anthropogenic factors. The last included cub that was shot by a Zapovednik forest guard in self defense, litter of cubs that were captured and removed from the wild after poachers killed their mother, litter of cub that almost certainly died after its mother disappeared (presumably poached), and litter of cubs that were kept alive by supplemental feeding from their 7th through th month after poachers killed their mother. Mean age at dispersal was months (n 5). Female and female did not disperse but settled in their natal home ranges. We only located female with her mother (female ) once between 5 and months of age, at which time female was poached. The mother of female was not collared, but tracks and observations indicated that they were not together after female was 7 8 months old. Of litters with unmarked cubs, cubs were never detected (via tracks or visual observation) in association with their radiocollared mother after 7 months of age. Reproductive rate was. cubs female year, but only half of these (.7 cubs/year) survived up to months of age. Assuming a female is reproductively active from 5 years of age, total lifetime productivity would be 5. cubs and total successful productivity would be 7.7 cubs. However, our data suggest that few, if any, females achieve such high lifetime productivity. Of the females monitored for this study, the status of is unknown (never collared, collar failure, and dispersal), 6 died at ages estimated to be years, and are still alive ( of these are also years). Only female survived the entire study period and beyond (January 99 December ). At years of age, she had produced 5 litters, with a lifetime production of at least 9 cubs but with only cubs surviving to months. At a reproductive rate of.8 cubs/year, she is well below our estimated average reproductive rate. DISCUSSION Although litters were born in all but months of the year (November, February, and March), tigers on our study site were seasonal breeders, with over 5% of all births occurring in late summer (August October) and corresponding conception rates peaking in March May. These results contradict the majority of literature on wild tiger populations that report peak conception rates in January and February (Baikov 95; Dunishenko and Kulikov 999; Kucherenko 985), suggesting a spring (April May) birth peak. Because these reports are based on observations made via snow tracking, the potential for bias is great because they had no information during snow-free months. Our data also contradict data from captive tigers, which demonstrated a distinct spring (April June) birth peak (Seal et al. 987). Indeed, our data contradict all other studies on all subspecies that report breeding throughout the year but with seasonal conception peaks in November early April and, hence, birth peaks in February July (reviews in Mazak 98; Nowell and Jackson 996; Table ). Small sample size and use of multiple births from individual tigers may have resulted in skewed estimates of birth and conception peaks in our study because multiple litters of some individual tigers tended to be produced at the same time of the year (i.e., female gave birth to litters in October and female gave birth to litters in August). Nonetheless, this data set represents one of the largest for a wild population of tigers, and the pattern coincides with birthing seasons of mountain lions (Puma concolor) in north-temperate environments (review in Logan and Sweanor ). Our results on other reproductive param- Downloaded from on August 8
7 9 JOURNAL OF MAMMALOGY Vol. 8, No. Subspecies Age at st reproduction (years) Bengal (captive) and Bengal 6 TABLE. Comparison among studies on reproductive parameters of tigers. Mean litter size Interbirth interval (months) Mean dispersal age (months) Litters (lifetime) Breeding season Birth season Reference March May January March January March January March Year round November April January February January February August October April June April June Year round February June This study Smith and McDougal (99), Smith (99) Seal et al., (987) Abramov K. (977), Abramov V. (96) Abramov K. (965) Kucherenko (97, 985) Matyushkin (98) Salmin (9) Smirnov (986) Smirnov and Miquelle (999) Nowell and Jackson (996, review), Mazak (98, review) Bragin (989) Matyushkin (98) E. N. Matyushkin et al. (in litt.) Salkina (99) Baikov (95) Dunishenko and Kulikov (999) Downloaded from on August 8
8 February KERLEY ET AL. REPRODUCTION AND AMUR TIGERS 95 eters of wild tigers also differed from those reported by many other observers (Table ). Mean birth interval (. months) was shorter than those in all previous reports for tigers (Table ) but almost identical to the.6 months reported by Smith and McDougal (99) for Bengal tigers. Mean litter size at st detection (.5 cubs) was at the high end of the range reported for tigers (Table ) but less than the nearly cubs/litter reported by Smith and McDougal (99). However, our estimate of litter size at months of age (.5 cubs) was at the low end of the range reported for tigers (Table ). This discrepancy with other reports for tigers is probably due to different methods used to measure reproductive parameters in the field. Radiotracking allowed us to estimate birth dates, birth intervals, litter sizes, and cub mortality more accurately than traditional snow tracking methodology because radiocollared tigers could be tracked continuously for long periods of time, including snow-free periods. Our results suggest that the reproductive potential of tigers is higher than was previously believed, i.e., birth intervals are shorter and mean litter size greater, but due to cub mortality, estimates of recruitment of young (survival to months) turned out to be similar to those of earlier reports (Abramov K. G. 965; Smirnov 986; E. N. Matyushkin et al., in litt.). Although our data may be more accurate than earlier studies, our inability to determine litter size during the st few months of life no doubt led to an underestimate of initial litter size and an underestimate of overall mortality rates of cubs. Even in captivity, mortality rates of nearly % have been reported during the first months of life (Christie and Walter ). Humancaused mortality, including poaching of mothers with cubs, accounted for 5% of all cub mortality identified during our study and is a primary factor depressing lifetime productivity of individuals and recruitment rates for the population (Kerley et al. ). On average, tigers in this study dispersed months earlier (9 versus months) than Bengal tigers in Nepal (Table ); although in Nepal, a cub s association with it s mother declined sharply after 8 months and most cubs were completely independent of their mothers by months. Higher tiger densities (/ km compared with./ km Smirnov and Miquelle 999; Sunquist 98) and the insular nature of the Nepal study area may have inhibited dispersal there. With the exception of birthing season and age at dispersal, reproductive parameters of female tigers on our study site were similar to those reported for Bengal tigers in Nepal (Smith and McDougal 99; Table ), where study techniques were similar to ours. This was true even though Bengal tigers occur where prey densities are an order of magnitude higher and tiger home ranges an order of magnitude smaller than those in the Russian Far East (Goodrich et al. 999; Miquelle et al. 999a; Smith et al. 987; Sunquist 98). Sunquist (98) estimated that lifetime production of a tigress living under optimum conditions in the wild could reach 8 animals and estimated that about half that number would likely reach adulthood. More recent data, both from Nepal and our work, suggest that such large reproductive outputs are seldom, if ever, met. Smith and McDougal (99) estimated mean lifetime reproduction of female tigers in Nepal at.5 dispersing young, and although our data do not allow precise calculations, it is clear that lifetime reproduction is even less in Russia. Thus, recent conclusions that tiger populations can grow rapidly and recover relatively rapidly from substantial losses (Sunquist et al. 999) may be overly optimistic. ACKNOWLEDGMENTS The Siberian Tiger Project is funded by The National Geographic Society, the Save The Tiger Fund, National Fish and Wildlife Foundation, the National Wildlife Federation, Exxon Corporation, the Charles Engelhard Foundation, Downloaded from on August 8
9 96 JOURNAL OF MAMMALOGY Vol. 8, No. Disney Wildlife Fund, Turner Foundation, and Richard King Mellon. We thank I. Nikolaev, B. Schleyer, N. Reebin, A. Reebin, A. Kostirya, I. Seerodkin, V. Melnikov, A. Saphonov, V. Schukin, and E. Gishko for their assistance with data collection. Director A. A. Astafiev and Assistant Director of Science M. N. Gromyko of Sikhote- Alin State Biosphere Zapovednik provided the logistical and administrative support necessary to conduct this work, and the Russian State Committee for Environmental Protection provided permits for capture, as well as much welcome political support, for our work. LITERATURE CITED ABRAMOV, K. G The tiger: a relic of the fauna of the Far East. Pp. 6 in Zapiski Primorskiy filiala Geographichiskaya Obshchestva SSSR. Dalnevostochniy Knizhniy Izdatilstva, Vladivostok, Russia (in Russian). ABRAMOV, K. G On the reproductive potential and numbers of the tiger. Zoologicheskii Zhurnal 56:68 75 (in Russian). ABRAMOV, V. K. 96. 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11 98 JOURNAL OF MAMMALOGY Vol. 8, No. Christie, and P. Jackson, eds.). Cambridge University Press, Cambridge, United Kingdom. WILLIAM, W., AND A. RABINOWITZ A global perspective on large carnivore conservation. Conservation Biology :6 5. YUDAKOV, A. G., AND I. G. NIKOLAEV Ecology of the tiger. Nauka, Moscow, Russia (in Russian). Submitted 5 September. Accepted May. Associate Editor was William L. Gannon. Downloaded from on August 8
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