LIU Peng 1, SUN Lixin 2, LI Jianli 3, WANG Li 2, ZHAO Wenge 1 and JIA Jingbo 3* 1. Introduction

Asian Herpetological Research 2010, 1(1): 48-56 DOI: 10.3724/SP.J.1245.2010.00048 Population Viability Analysis of Gloydius shedaoensis from Northeastern China: A Contribution to the Assessment of the Conservation and Management Status of an Endangered Species LIU Peng 1, SUN Lixin 2, LI Jianli 3, WANG Li 2, ZHAO Wenge 1 and JIA Jingbo 3* 1 College of Life Sciences and Technology, Harbin Normal University, Harbin 150025, Heilongjiang, China 2 Administrative Office of Snake Island and Laotie Mountain Nature Reserve, Dalian 116041, Liaoning, China 3 College of Wildlife Resources, Northeast Forestry University, Harbin 150040, Heilongjiang, China Abstract Shedao pit-vipers (Gloydius shedaoensis) on Snake Island in the Liaoning Province, China, are among the most imperiled species in China. The isolated and unique populations are crucial in the recovery of this endangered species by providing a way for conservation and management. Research based on the ecological simulation tools can evaluate alternative mitigation strategies in terms of their benefits to the populations, which are vital for informed decision-making. In this paper, using the program VORTEX 9.42, we developed a population viability analysis (PVA) for the Shedao pit-viper to: (1) address the extinction likelihood of the population; (2) simulate population dynamics under various environment events, and (3) evaluate the efficacy of current protection and management strategies. Overall, we found the population to be susceptible to the factors of catastrophic events, mortality and environment capacity. The population is recovering slowly at present on account of improvement of habitat and greater food availability. Under the current conditions, the probability of extinction in 100 years is approximately zero. These data coincide with the evidence that the wild population may be arriving at K. Our results strengthen the view that protection and management can create a pronounced effect on populations of this endangered species. Keywords Gloydius shedaoensis, VORTEX simulation model, sensitivity analysis, model veracity test, species conservation 1. Introduction The persistence of species on oceanic islands has played an important role in the development of ecological theory, especially in the field of biogeography and conservation biology (McArthur and Wilson, 1967). A number of island species present pressing conservation problems due to their unique adaptations, their limited ability to compete with non-native species, their geographic isolation, and their vulnerability to localized stochastic events (Kohlmann et al., 2005). An example is the Shedao pit-viper (Gloydius shedaoensis). Because the population has experienced pre- *Corresponding author: Dr. JIA Jingbo, from University of Helsinki, Finland in 1996. Now working as professor and dean in the College of Wildlife Resources, NEFU, with his research focusing on conservation biology and wildlife ecology/management. E-mail: mynian25@hotmail.com Received: 29 May 2010 Accepted: 14 July 2010 cipitous declines in the recent years, due to restricted distribution and low population size, it has been classified in the Vulnerable category in the China Red Data Book of Endangered Animals: Amphibia and Reptilia (1998) and in the Critically Endangered category of the China Species Red List (2004). Therefore, Chinese biologists have accorded a high conservation priority to this species, and have studied it for approximately 30 years since the Liaoning Snake Island and Laotie Mountain National Nature Reserve was founded in 1980. Major results from the studies on the Shedao pit-viper have been published by Chinese specialists (Wu, 1977; Zhao, 1979; Jiang and Zhao, 1980; Yang, 1983; Huang, 1984; Yang and Ma, 1986; Huang, 1989; Li et al., 1990; Sun et al., 1990; Sun et al., 1993; Li, 1995; Sun et al., 2000; Sun et al., 2001; Sun et al., 2002; Li et al., 2007) and in recent years, Rick Shine has done a substantial amount of work on the Snake Island endemic (Shine and Sun, 2002; Shine et al., 2002a; Shine et al., 2002b; Shine et al., 2002c). These

No. 1 LIU Peng et al. Population Viability Analysis of Gloydius shedaoensis 49 studies focus on (1) morphology, taxonomy, distribution; (2) population ecology, reproductive ecology, behavior ecology; and (3) species protection and resource utilization. Despite a substantial amount of resources and time devoted to protecting and managing the population, information on its conservation biology is rather sketchy. The effectiveness of these conservation actions is difficult to estimate because the relative paucity of data for the Shedao pit-viper and the uncertainty of many relevant parameters (e.g., the frequency and severity of environment events and self-life history characters). In the present study, we demonstrate, using the Shedao pit-viper population on the Snake Island as a case study, how criteria can be formulated and an analysis performed to search for an answer based on more than intuition, whether the current conservation efforts and management strategies have been effective in the protection and restoration of the island snakes in the past 30 years, how the fate of this population is in future, and what key factors will affect population increase. Population viability analysis (PVA) is a tool used in conservation biology with a population dynamics model to answer these questions (Brook et al., 2000). It includes an array of quantitative methods and the program VOR- TEX is a commonly used modeling tool (Boyce, 1992; Lindenmayer and Possingham, 1996; Beissinger and Westphal, 1998). In this study, we analyzed an extensive dataset to simulate variance of the Shedao pit-viper population size on Snake Island, estimate the probabilities of extinction events and to assess the efficacy of developing conservation and management strategies for the endangered species in China. 2. Study Area and Species The island of Shedao (Snake Island), also known as Xiaolongshan (Little Dragon Mountain), lies in the Bohai Sea, 13 km off the southern end of Liaodong Peninsula in northeastern China (38º57 N, 120º59 E) (Figure 1). This small island is 1.7 km long, 0.7 km wide and covers approximately 0.73 km 2, with elevations ranging from 0 to 648 m. The climate is cool-temperate, with mean monthly air temperatures averaging 24.0 ºC in midsummer (July) and 4.1 ºC in midwinter (January), and a mean annual rainfall of 31 cm (Huang, 1989). It has steep and rocky outcrops on the island, with a covering of grasslands, low scrub and woodlands (Shine and Sun, 2002). The island lies on a major migration route for Asian birds that overwinter in southern Asia but breed in Siberia (Sun et al., 2001), and because of its geographic location, the island serves as a stepping-stone for migrating birds during spring (May) and autumn (September October) each year (Li, 1995). Figure 1 Location of Snake Island in Liaoning, China Nature Reserve: The Snake Island and Laotie Mountain National Nature Reserve The Shedao pit-viper, G. shedaoensis, is the only herpetofaunal species on the island. Adults of both sexes average approximately 650 mm snout-vent length (SVL) (Figure 2). The snakes have highly toxic venom (Zhao et al., 1979) and are inactive throughout most of the year, but emerge to lie in wait for prey during two bird-migration periods (Sun et al., 1990). Adult pit-viper feed almost exclusively on migrating birds from ambush sites rather than by active searching (Sun et al., 2001; Shine and Sun, 2002), whereas juvenile snakes feed on centipedes as well as small birds (Huang, 1984; Li, 1995). The Shedao pit-viper attains remarkably high population densities on the island, with up to one snake per m 2 in suitable habitat (Sun et al., 2001), as no natural predators occur in sympatry (Li, 1995). Figure 2 An adult of G.. shedaoensis 3. Material and Methods 3.1 History of the population Culling statistics indicate that in 1973 there must have been at least 20 000

50 Asian Herpetological Research Vol. 1 Shedao pit-vipers on Snake Island, with an increase to 28 321 in 1980. Habitat destruction and over harvesting on the island resulted in a decrease in population size in 1982 (Huang, 1984). Population numbers increased gradually, from 10 009 in 1982 to 20 281 in 2005, which may be attributed to effective management by the nature reserve (Sun et al., 2007) (Figure 3). Figure 3 Fluctuations in G. shedaoensis population from 1973 to 2005 3.2 PVA software We used VORTEX, version 9.42 to simulate the dynamics of the Shedao pit-viper population (Lacy et al., 2003). We simulated the population for 100 years and reported intervals at 10 years from 1982 as the beginning for when data were reliable (Huang, 1984), repeating each run 500 times. 3.3 Demography Whenever possible, we estimated some parameters required by VORTEX from original observations and previous intensive studies on Shedao pit-viper or with personal experience of the authors. Other data were derived mainly from the literature and the author s knowledge of other species. The parameters used in the computer simulation model are provided as follows: The life history We assumed that the Shedao pit-viper population on Snake Island started as a stable age distribution rather than a not specifying an age distribution due to a lack of data. Mating system for the Shedao pit-viper was polygynous (Yang, 1983), sex ratio at birth was 1:1, minimum male and female breeding age was 3 years, maximum clutch size was 8, maximum breeding age 7 years and life span was 10 years (Huang, 1989). Mating monopolization We assumed that not all males bred and the percent total male are 70%. The number percentage of progenitive female in total female is P (N), N is population size. When N=0, that is original population, P (0) density dependence term is 70% and N=k, that is environmental capacity, P (K) density dependence term is 20%. Environmental variation Proportion of reproducing and mortality rates were correlated, so it might be density dependent breeding. Density dependence term B is 2 and female mating depress term A is 2. We assumed that EV (reproduction) is correlated with EV (survival) and they were given a standard deviation of 0.5 of their respective mean. Inbreeding depression To account for having no the previous inbreeding history of the population, all simulations were started with more individuals and low genetic diversity (Ujvari et al., 2002), so our simulations began with no inbreeding depression. Transfer and diffusion Within the enclosed island ecosystem, there is no dispersal among the Shedao pit-viper population. The gene flow of this species from one ridge to another exists in the seven subpopulations of G. shedaoensis, though the migration is very slowly. So we supposed that all the male and female Shedao pit-viper can migrate between the subpopulations, and we assume the diffuse of dispersal to be 5% and survival of dispersal to be 100%. Furthermore, for the first ditch and the sixth ditch are disconnection, we assume that they have no dispersal. And simultaneously, steep slope is in the west of the Snake Island, thus we assume it does not transfer among other subpopulations. Mortality There are no notable differences in G. shedaoensis mortality between males and females, according to the literature, from which the mean adult mortality is 5.27% and the juvenile mortality is 44.39% (Sun et al., 2000). Therefore, we estimate the mortality and SD of G. shedaoensis in different age groups (Table 1). Table 1 Mortality of G. shedaoensis in different age groups Age Mortality % SD 0~1 40 10 1~2 20 5 2~3 10 3 Adult 5 1 Catastrophes VORTEX allows the user to change the frequency at which catastrophic events occur, and their severity in regard to successful reproduction and mortality. Drought, fire and typhoon were most of the calamities that Shedao pit-vipers would be exposed to based on climate data. Drought happens frequently and its effect on the population of G. shedaoensis is the most severe. Typhoons happen rarely, but their effect is more severe than fire (Sun et al., 2000). Thus, we assumed that

No. 1 LIU Peng et al. Population Viability Analysis of Gloydius shedaoensis drought, fire and typhoons happened 20, 2 and 1 times every 100 years with frequencies of 20%, 2% and 1%, which make a 20%, 5% and 10% increase in mortality and 40%, 10% and 20% decrease in reproduction, respectively (Table 2). Table 2 Effect of regional stochastic events on the population of G. shedaoensis Frequency % Unsuccessful reproduction % Mortality % Drought 20 40 20 Fire 2 10 5 Typhoon 1 20 10 Type of catastrophes Environmental capacity The Shedao pit-viper population on Snake island was represented as a seven-element metapopulation (Six ditches comprising subpopulations Ⅰ-Ⅵ and one steep that is subpopulation Ⅶ) (Figure 4). Because the data from 1982 were exact, each number of subpopulations can be confirmed as the original data in the model. Based on the suitable habitat and food availability, we can estimate the environmental capacity (K) of the seven G. shedaoensis subpopulations (Table 3). We supposed that K changed every 5 years and percent change was 10%. 51 Table 3 Environmental capacity of seven subpopulations of G. shedaoensis Subpopulation Original number Environmental capacity (K) SD Ⅰ Ⅱ 1566 3224 Ⅲ Ⅳ Ⅴ 425 636 742 Ⅵ Ⅶ 1748 1668 3000 4500 1000 1200 1400 3500 3000 250 500 100 100 100 200 300 Natural enemy Adult pit-vipers on the island appear to have no natural predators, but juvenile snakes are sometimes killed by sparrow hawks (Li, 1995). This happens at lower frequency; hence it most likely has a negligible impact on the population. 3.4 Veracity test In order to validate the veracity of the model, we compared the fitting results of the model output in 2005 with the observation value in 2005 (Li et al., 2007). 3.5 Sensitivity analysis Sensitivity analysis is a quantitative assessment of the population response (e.g., the change in the population growth rate or extinction risk) when a parameter in the model is altered. Therefore, in the present study, we selected five model parameters (catastrophes, harvest, transfer, environmental capacity and mortality) for our sensitivity analysis. We conducted that with environmental capacity reduced by 50%, 20 snakes (10 males, 10 females) captured per year and mortality increased by 10%, catastrophes and transfer both happened, while holding all other parameters constant. We compared the model simulation results with ideal condition (no mating monopolization, density dependence, catastrophes and inbreeding depression). 4. Results 4.1 Population dynamics under ideal conditions Using the model, we calculated that the intrinsic rate of increase (rm) averaged 0.005, finite growth rate (λ) = 1.005, net reproductive rate (R0) = 1.104 under the ideal condition. Generation length of G. shedaoensis is 4.9 years for both male and female that means the population gene will be updating every 4.9 years. Figure 4 Landform and regionalization map of the Snake Island based on six ditches (Ⅰ-Ⅵ) and one steep (Ⅶ) Harvest and supplement Poaching was strictly forbidden and no hunting took place in the nature reserve. 4.2 Model veracity test The fitting results of the model output in 2005 are 12.7% higher than the actual number of metapopulations (Table 4), but since some numbers would have been missed during field research, we consider that the veracity model is good. 4.3 Population dynamics under the simulated conditions Simulating the Shedao pit-viper population with VORTEX

52 Asian Herpetological Research Vol. 1 Table 4 Predicted value and actual numbers of subpopulations and the metapopulation of G. shedaoensis in 2005 Subpopulation Ⅰ Ⅱ Ⅲ Ⅳ Ⅴ Ⅵ Ⅶ Metapopulation Model predicted value 3614 5129 1400 1659 1886 5216 3623 23229 Actual number 2494 5075 986 1204 1800 5123 3599 20281 Number difference 1120 54 414 455 86 93 24 2948 Percent difference 31% 1% 30% 27% 4.6% 1.8% 0.7% 12.7% revealed a steadily increasing population (r = 0.03, SD = 0.057). Under actual conditions, the probability of extinction is zero in 100 years for any subpopulations, and population size is fluctuating with environmental capacity (K) after 20 years from 1982 (Figure 5). 4.4 Effects of five environmental factors The results show that the number of populations would attain to environmental capacity (K) in a short period of time since 1982; capacity did not change remarkably with harvesting and transfer that we have supposed in part 3.3 and 3.5, but did reduce if catastrophes happened and had a 10% increase in mortality. When environmental capacity reduced by 5%, the population size would reach and keep a lower level for a longer period of time. It is noteworthy that five factors happened at the same time, it would make the population reduce quickly in shorter time (Figure 6). 5. Discussion 5.1 Conservation of snakes In a recent overview of snake conservation, we note that snakes attract human attention when a person is bitten or snakes become the cause of a natural catastrophe (e.g., the decimation of an endangered bird community). When it comes to negative aspects happening to snakes, few resources for support are available (Dodd, 1993). Although this view is, unfortunately, still typical, conservationists have started to develop plans and research programs for endangered snake populations, not only in the more affluent countries of Europe and North America (Corbett, 1989), but also in the developing countries of Asia (Bhupathy and Vijayan, 1989; Filippi and Luiselli, 2000) and Africa (Akani et al., 1999). Many snake populations are declining because of habitat loss (Kjoss and Litvaitis, 2001), commercialization Figure 5 Simulated population trajectories for seven subpopulations and metapopulation of G. shedaoensis on Snake Island, from VOR- TEX simulation with no catastrophes or management actions in 100 years.

No. 1 LIU Peng et al. Population Viability Analysis of Gloydius shedaoensis 53 Figure 6 Population dynamics of G. shedaoensis by different factors from 1982 and use (Alves and Pereira, 2007), the impact of hunting (Brooks et al., 2007), and illegal collection for the pet trade (Filippi and Luiselli, 2000; Webb et al., 2002). Furthermore, certain biological characteristics increase vulnerability and likelihood of extinction: low reproductive success, high habitat and dietary specialization, and low dispersal rates. Snakes with slow life history patterns are more prone to extinction because some of their reproductive traits (low reproductive frequency, small clutches) limit recruitment rates and restrain population growth (Pleguezuelos et al., 2007). In China, government and civilians are paying attention to protect and manage snakes (Zhou and Jiang, 2004). However, the conservation and management of endangered snakes in field are likely to be complex, and simple data and model may prove to be elusive. Nonetheless, we think that new ways of studying snake populations have the potential to reveal important insights into snake conservation biology. 5.2 PVA used in Shedao pit-viper Population viability analysis (PVA) is a suitable tool with detailed data and extended research, otherwise it may be misleading (Beissinger et al., 2002). To our knowledge, however, no studies have directly simulated snake population dynamics and determined their impact on population viability. Without such studies, it is difficult to evaluate the status that conservation and management has on snake populations. Indeed, the Shedao pit-viper has been suitable for such a study, compared to other snakes in China. First, the Shedao pit-viper satisfies all of the conditions with the following characteristics: the snakes are large; they exist at a high density; they occupy a relatively open, homogeneous habitat; they are sedentary rather than migratory; they are easily observable when active, but totally hidden when inactive; and they do not flee from human presence (Sun, et al, 2001). Second, the survey data from the island provides the most extensive dataset ever gathered on the Shedao pit-viper population in Chinese snakes. Third, the species is considered the most endangered snake in China under its current conservation status. Thus, PVA such as ours may help to predict which segments of the snake population are most at risk, and which times and places are likely to be most important in this respect. We also seek to compile sound information that can be applied in conservation planning for the species. The results also illustrate the importance of including a long-term perspective in modeling threatened populations. 5.3 Effect factors of Shedao pit-viper population dynamic Based on previous studies on the Shedao pit-viper and on other snake species, our results through PVA of the Shedao pit-viper population with the computer model showed that the followed factors can lead to snake population dynamics: Catastrophes Although population estimation for conservation purposes would not be accurate in the present example, the frequency and severity of environmental

54 Asian Herpetological Research Vol. 1 variation, such as a typhoon, drought or large fire are potentially important factors determining the fate of the island snake. With knowledge of the probability and destructive extent of catastrophes for the population, there is a reasonably sound basis for assessing the severity of a severe catastrophe, and we are still being able to monitor the changes within the population. Harvest In the present study, the precautionary principle suggests that no deliberate harvest is acceptable for endangered species. Based on this criterion, the results suggest that only a very limited amount of harvest should be permitted at low population sizes. Proper collecting for research is acceptable and will not affect the population increase. But, if the population drops below the threshold, harvesting must cease until the population reaches or exceeds the threshold again. Thus, predicting the time and numbers about when and whether snakes will be taken, environmental capacity (K) can be of value in reducing the risk of over harvest by reasonable utilization to avoid wastage. Inbreeding depression Inbreeding depression should also be integrated in demographic risk assessment and important effects of inbreeding depression may be concealed. If the ditch on the island can act as significant barriers to gene flow, which can ultimately reduce the overall genetic diversity of populations and not increase the risk for extinction. So it is therefore important that studies incorporate gene flow and diversity of the subpopulations of G. shedaoensis on the island to make accurate predictions about the impacts of inbreeding depression on animal populations. Environmental capacity decreasing Although the habitat on the island is broadly homogeneous, subtle spatial variation in aspects such as slope, elevation, and vegetation cover undoubtedly influence factors such as the availability of prey or foraging sites, wind speed, temperature and relative humidity. All of these factors may affect the size and structure of the population increasing in future. 5.4 Testing and using the model Clearly, estimates of such parameters can be substantially affected by habitat conditions and population status. Although the validity of this model has been verified for G. shedaoensis on the island, no validation has been conducted for other snakes or larger-bodied reptiles. Hence, uncritical use of such data, without an understanding of the criterion in which census conditions affect parameter estimates, can lead to serious error. On the other hand, our study also suggests that many of these biases are sufficiently consistent that they can readily be taken into account. Thus, modeling may provide valuable insights into biological attributes of the study population, but must be used with great care. Our next study demonstrates how these data can be taken into account in PVA simulations and how this model can be applied in the other endangered species. 5.5 G. shedaoensis population persistence At present, G. shedaoensis enjoys a certain degree of protection, and has a better basis of scientific research and management means. Despite its large populations size on Snake Island (although with very limited areas), the Shedao pit-viper has, until recently, has been the most endangered vipers in China. Such lack of information is probably a consequence of the researchers scarcity and the discreet habitat of this viper. We conclude that the population of G. shedaoensis is currently at a critically low but increasing level; thus, population viability of the species in a long period appears possible. Overall, our analyses provide both a cautionary tale and encouragement for conservation biologists who use census data and model to estimate population size and endangered status of their study organisms. Moreover, in the study of snake status, we identified the Shedao pit-viper among the priorities for conservation. 5.6 Management implications On the one hand, fluctuations of the environment interfere with the island ecosystems. On the other, they lose their genetic diversity due to limited dispersal. Correct handling of the relationships between people, snakes and birds, the relations between protection and economic development, intensifying research and effective management, and raising the public s awareness of protection are effective ways of protecting the G. shedaoensis population and restoring its resources. 6. Conclusions The loss of many animal species throughout the world is inevitable and apparently unavoidable. In other instances, perpetuation of a species can be achieved only by expenditure of a prohibitively large sum of money. In view of the Shedao pit-viper s value to medicine and the apparent suitability of this animal for laboratory life, it would be fatuous negligence to allow this species to become extinct when so little is required to ensure its survival. The existing management measures set by the nature reserve can assure that this population stabilizes at a level

No. 1 LIU Peng et al. Population Viability Analysis of Gloydius shedaoensis 55 of environmental capacity for a long time, which makes the extinction probability of this population to 0 within 100 years. The main factors of affecting population dynamics are environmental capacity, mortality and catastrophes. At the level of environmental capacity, there will be no large impact on population dynamics of G. shedaoensis when captured properly. Increasing the environmental capacity and reducing the mortality are the main measures of increasing the population number of G. shedaoensis. So these will be an important work contents of nature reserve in future. Acknowledgements We thank our colleagues on Snake Island and at Laotie Mountain National Nature Reserve in Liaoning (especially Wu Yuqun, Lin Xizhen) who facilitated our work on the Island. We also thank Wang Xiaoping, Wang Liping, Bi Hengtao, Wu Chao, Qu Nanxi, Yu Yefei who have helped us with fieldwork over the years. 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