Asian Herpetological Research 2010, 1(1): 48-56 DOI: 10.3724/SP.J.1245.2010.00048

Population Viability Analysis of shedaoensis from North- eastern China: A Contribution to the Assessment of the Conser- vation and Management Status of an Endangered

LIU Peng1, SUN Lixin 2, LI Jianli3, WANG Li2, ZHAO Wenge1 and JIA Jingbo3* 1 College of Life Sciences and Technology, Harbin Normal University, Harbin 150025, Heilongjiang, China 2 Administrative Office of 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 deci- sion-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 evi- dence 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 cipitous declines in the recent years, due to restricted distribution and low population size, it has been classified The persistence of species on oceanic islands has played in the Vulnerable category in the China Red Data Book an important role in the development of ecological theory, of Endangered : Amphibia and Reptilia (1998) especially in the field of biogeography and conservation and in the Critically Endangered category of the China biology (McArthur and Wilson, 1967). A number of is- Species Red List (2004). Therefore, Chinese biologists land species present pressing conservation problems due have accorded a high conservation priority to this species, to their unique adaptations, their limited ability to com- and have studied it for approximately 30 years since the pete with non-native species, their geographic isolation, Liaoning Snake Island and Laotie Mountain National and their vulnerability to localized stochastic events Nature Reserve was founded in 1980. Major results from (Kohlmann et al., 2005). the studies on the Shedao pit-viper have been published An example is the Shedao pit-viper (Gloydius she- by Chinese specialists (Wu, 1977; Zhao, 1979; Jiang and daoensis). Because the population has experienced pre- Zhao, 1980; Yang, 1983; Huang, 1984; Yang and Ma,

1986; Huang, 1989; Li et al., 1990; Sun et al., 1990; Sun *Corresponding author: Dr. JIA Jingbo, from University of Helsinki, et al., 1993; Li, 1995; Sun et al., 2000; Sun et al., 2001; Finland in 1996. Now working as professor and dean in the College of Sun et al., 2002; Li et al., 2007) and in recent years, Rick Wildlife Resources, NEFU, with his research focusing on conservation Shine has done a substantial amount of work on the biology and wildlife ecology/management. E-mail: [email protected] Snake Island endemic (Shine and Sun, 2002; Shine et al., Received: 29 May 2010 Accepted: 14 July 2010 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, , distribution; 2001), and because of its geographic location, the island (2) population ecology, reproductive ecology, behavior serves as a stepping-stone for migrating birds during ecology; and (3) species protection and resource utiliza- spring (May) and autumn (September–October) each year tion. Despite a substantial amount of resources and time (Li, 1995). devoted to protecting and managing the population, in- formation on its conservation biology is rather sketchy. The effectiveness of these conservation actions is diffi- cult 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 environ- ment events and self-life history characters). In the pre- sent study, we demonstrate, using the Shedao pit-viper population on the Snake Island as a case study, how cri- teria 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 resto- ration of the island in the past 30 years, how the Figure 1 Location of Snake Island in Liaoning, China Nature Reserve: The Snake Island and Laotie Mountain National fate of this population is in future, and what key factors Nature Reserve will affect population increase. Population viability analysis (PVA) is a tool used in The Shedao pit-viper, G. shedaoensis, is the only her- conservation biology with a population dynamics model petofaunal species on the island. Adults of both sexes to answer these questions (Brook et al., 2000). It includes average approximately 650 mm snout-vent length (SVL) an array of quantitative methods and the program VOR- (Figure 2). The snakes have highly toxic venom (Zhao et TEX is a commonly used modeling tool (Boyce, 1992; al., 1979) and are inactive throughout most of the year, Lindenmayer and Possingham, 1996; Beissinger and but emerge to lie in wait for prey during two Westphal, 1998). In this study, we analyzed an extensive bird-migration periods (Sun et al., 1990). Adult pit-viper dataset to simulate variance of the Shedao pit-viper feed almost exclusively on migrating birds from ambush population size on Snake Island, estimate the probabili- sites rather than by active searching (Sun et al., 2001; ties of extinction events and to assess the efficacy of de- Shine and Sun, 2002), whereas juvenile snakes feed on veloping conservation and management strategies for the centipedes as well as small birds (Huang, 1984; Li, 1995). endangered species in China. The Shedao pit-viper attains remarkably high population densities on the island, with up to one snake per m2 in 2. Study Area and Species suitable habitat (Sun et al., 2001), as no natural predators occur in sympatry (Li, 1995). 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 ap- proximately 0.73 km2, 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 Figure 2 An adult of G.. shedaoensis rainfall of 31 cm (Huang, 1989). It has steep and rocky outcrops on the island, with a covering of grasslands, low 3. Material and Methods scrub and woodlands (Shine and Sun, 2002). The island 3.1 History of the population Culling statistics indi- lies on a major migration route for Asian birds that over- cate that in 1973 there must have been at least 20 000 winter in southern Asia but breed in Siberia (Sun et al., 50 Asian Herpetological Research Vol. 1

Shedao pit-vipers on Snake Island, with an increase to is 20%. 28 321 in 1980. Habitat destruction and over harvesting Environmental variation Proportion of reproducing on the island resulted in a decrease in population size in and mortality rates were correlated, so it might be density 1982 (Huang, 1984). Population numbers increased dependent breeding. Density dependence term B is 2 and gradually, from 10 009 in 1982 to 20 281 in 2005, which female mating depress term A is 2. We assumed that EV may be attributed to effective management by the nature (reproduction) is correlated with EV (survival) and they reserve (Sun et al., 2007) (Figure 3). 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 simula- tions 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

Figure 3 Fluctuations in G. shedaoensis population from 1973 to G. shedaoensis, though the migration is very slowly. So 2005 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 3.2 PVA software We used VORTEX, version 9.42 to dispersal to be 100%. Furthermore, for the first ditch and simulate the dynamics of the Shedao pit-viper population the sixth ditch are disconnection, we assume that they (Lacy et al., 2003). We simulated the population for 100 have no dispersal. And simultaneously, steep slope is in years and reported intervals at 10 years from 1982 as the the west of the Snake Island, thus we assume it does not beginning for when data were reliable (Huang, 1984), transfer among other subpopulations. repeating each run 500 times. Mortality There are no notable differences in G. 3.3 Demography Whenever possible, we estimated shedaoensis mortality between males and females, ac- some parameters required by VORTEX from original cording to the literature, from which the mean adult mor- observations and previous intensive studies on Shedao tality is 5.27% and the juvenile mortality is 44.39% (Sun pit-viper or with personal experience of the authors. et al., 2000). Therefore, we estimate the mortality and SD Other data were derived mainly from the literature and of G. shedaoensis in different age groups (Table 1). the author’s knowledge of other species. The parameters used in the computer simulation model are provided as Table 1 Mortality of G. shedaoensis in different age groups follows: Age Mortality % SD The life history We assumed that the Shedao pit-viper 0~1 40 10 population on Snake Island started as a stable age distri- 1~2 20 5 bution rather than a not specifying an age distribution due 2~3 10 3 to a lack of data. Mating system for the Shedao pit-viper Adult 5 1 was polygynous (Yang, 1983), sex ratio at birth was 1:1, minimum male and female breeding age was 3 years, Catastrophes VORTEX allows the user to change the maximum clutch size was 8, maximum breeding age 7 frequency at which catastrophic events occur, and their years and life span was 10 years (Huang, 1989). severity in regard to successful reproduction and morta- Mating monopolization We assumed that not all males lity. Drought, fire and typhoon were most of the calami- bred and the percent total male are 70%. The number ties that Shedao pit-vipers would be exposed to based on percentage of progenitive female in total female is P (N), climate data. Drought happens frequently and its effect N is population size. When N=0, that is original popula- on the population of G. shedaoensis is the most severe. tion, P (0) density dependence term is 70% and N=k, that Typhoons happen rarely, but their effect is more severe is environmental capacity, P (K) density dependence term than fire (Sun et al., 2000). Thus, we assumed that No. 1 LIU Peng et al. Population Viability Analysis of Gloydius shedaoensis 51 drought, fire and typhoons happened 20, 2 and 1 times Table 3 Environmental capacity of seven subpopulations of G. every 100 years with frequencies of 20%, 2% and 1%, shedaoensis which make a 20%, 5% and 10% increase in mortality Subpopulation Ⅰ Ⅱ Ⅲ Ⅳ Ⅴ Ⅵ Ⅶ and 40%, 10% and 20% decrease in reproduction, respec- Original number 1566 3224 425 636 742 1748 1668 Environmental tively (Table 2). 3000 4500 1000 1200 1400 3500 3000 capacity (K)

SD 250 500 100 100 100 200 300 Table 2 Effect of regional stochastic events on the population of

G. shedaoensis Natural enemy Adult pit-vipers on the island appear to Frequency Unsuccessful Mortality Type of catastrophes % reproduction % % have no natural predators, but juvenile snakes are some- Drought 20 40 20 times killed by sparrow hawks (Li, 1995). This happens Fire 2 10 5 at lower frequency; hence it most likely has a negligible Typhoon 1 20 10 impact on the population. 3.4 Veracity test In order to validate the veracity of the Environmental capacity The Shedao pit-viper popula- model, we compared the fitting results of the model out- tion on Snake island was represented as a seven-element put in 2005 with the observation value in 2005 (Li et al., metapopulation (Six ditches comprising subpopulations 2007). Ⅰ-Ⅵ and one steep that is subpopulation Ⅶ) (Figure 4). 3.5 Sensitivity analysis Sensitivity analysis is a quan- Because the data from 1982 were exact, each number of titative assessment of the population response (e.g., the subpopulations can be confirmed as the original data in change in the population growth rate or extinction risk) the model. Based on the suitable habitat and food avai- when a parameter in the model is altered. Therefore, in lability, we can estimate the environmental capacity (K) the present study, we selected five model parameters (ca- of the seven G. shedaoensis subpopulations (Table 3). We tastrophes, harvest, transfer, environmental capacity and supposed that K changed every 5 years and percent mortality) for our sensitivity analysis. We conducted that change was 10%. with environmental capacity reduced by 50%, 20 snakes (10 males, 10 females) captured per year and mortality increased by 10%, catastrophes and transfer both hap- pened, while holding all other parameters constant. We compared the model simulation results with ideal condi- tion (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. 4.2 Model veracity test The fitting results of the model

output in 2005 are 12.7% higher than the actual number Figure 4 Landform and regionalization map of the Snake Island of metapopulations (Table 4), but since some numbers based on six ditches (Ⅰ-Ⅵ ) and one steep (Ⅶ) would have been missed during field research, we con-

sider that the veracity model is good. Harvest and supplement Poaching was strictly for- bidden and no hunting took place in the nature reserve. 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 = 5. Discussion 0.057). Under actual conditions, the probability of extinc- tion is zero in 100 years for any subpopulations, and 5.1 Conservation of snakes In a recent overview of population size is fluctuating with environmental capa- snake conservation, we note that snakes attract human city (K) after 20 years from 1982 (Figure 5). attention when a person is bitten or snakes become the 4.4 Effects of five environmental factors The results cause of a natural catastrophe (e.g., the decimation of an show that the number of populations would attain to en- endangered bird community). When it comes to negative vironmental capacity (K) in a short period of time since aspects happening to snakes, few resources for support 1982; capacity did not change remarkably with harves- are available (Dodd, 1993). Although this view is, unfor- ting and transfer that we have supposed in part 3.3 and tunately, still typical, conservationists have started to de- 3.5, but did reduce if catastrophes happened and had a velop plans and research programs for endangered snake 10% increase in mortality. When environmental capacity populations, not only in the more affluent countries of reduced by 5%, the population size would reach and keep Europe and North America (Corbett, 1989), but also in the a lower level for a longer period of time. It is noteworthy developing countries of Asia (Bhupathy and Vijayan, 1989; that five factors happened at the same time, it would Filippi and Luiselli, 2000) and Africa (Akani et al., 1999). make the population reduce quickly in shorter time Many snake populations are declining because of habi- (Figure 6). tat 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 the Shedao pit-viper satisfies all of the conditions with (Brooks et al., 2007), and illegal collection for the pet the following characteristics: the snakes are large; they trade (Filippi and Luiselli, 2000; Webb et al., 2002). Fur- exist at a high density; they occupy a relatively open, thermore, certain biological characteristics increase vul- homogeneous habitat; they are sedentary rather than mi- nerability and likelihood of extinction: low reproductive gratory; they are easily observable when active, but to- success, high habitat and dietary specialization, and low tally hidden when inactive; and they do not flee from dispersal rates. Snakes with ‘‘slow’’ life history patterns human presence (Sun, et al, 2001). Second, the survey are more prone to extinction because some of their re- data from the island provides the most extensive dataset productive traits (low reproductive frequency, small ever gathered on the Shedao pit-viper population in Chi- clutches) limit recruitment rates and restrain population nese snakes. Third, the species is considered the most growth (Pleguezuelos et al., 2007). endangered snake in China under its current conservation In China, government and civilians are paying atten- status. tion to protect and manage snakes (Zhou and Jiang, 2004). Thus, PVA such as ours may help to predict which However, the conservation and management of endan- segments of the snake population are most at risk, and gered snakes in field are likely to be complex, and simple which times and places are likely to be most important in data and model may prove to be elusive. Nonetheless, we this respect. We also seek to compile sound information think that new ways of studying snake populations have that can be applied in conservation planning for the spe- the potential to reveal important insights into snake con- cies. The results also illustrate the importance of inclu- servation biology. ding a long-term perspective in modeling threatened populations. 5.2 PVA used in Shedao pit-viper Population viability analysis (PVA) is a suitable tool with detailed data and 5.3 Effect factors of Shedao pit-viper population dy- extended research, otherwise it may be misleading namic Based on previous studies on the Shedao (Beissinger et al., 2002). To our knowledge, however, no pit-viper and on other snake species, our results through studies have directly simulated snake population dyna- PVA of the Shedao pit-viper population with the com- mics and determined their impact on population viability. puter model showed that the followed factors can lead to Without such studies, it is difficult to evaluate the status snake population dynamics: that conservation and management has on snake popula- Catastrophes Although population estimation for con- tions. Indeed, the Shedao pit-viper has been suitable for servation purposes would not be accurate in the present such a study, compared to other snakes in China. First, example, the frequency and severity of environmental 54 Asian Herpetological Research Vol. 1 variation, such as a typhoon, drought or large fire are that many of these biases are sufficiently consistent that potentially important factors determining the fate of the they can readily be taken into account. Thus, modeling island snake. With knowledge of the probability and de- may provide valuable insights into biological attributes of structive extent of catastrophes for the population, there the study population, but must be used with great care. is a reasonably sound basis for assessing the severity of a Our next study demonstrates how these data can be taken severe catastrophe, and we are still being able to monitor into account in PVA simulations and how this model can the changes within the population. be applied in the other endangered species. Harvest In the present study, the precautionary princi- 5.5 G. shedaoensis population persistence At present, ple suggests that no deliberate harvest is acceptable for G. shedaoensis enjoys a certain degree of protection, and endangered species. Based on this criterion, the results has a better basis of scientific research and management suggest that only a very limited amount of harvest should means. Despite its large populations size on Snake Island be permitted at low population sizes. Proper collecting (although with very limited areas), the Shedao pit-viper for research is acceptable and will not affect the popula- has, until recently, has been the most endangered vipers tion increase. But, if the population drops below the in China. Such lack of information is probably a conse- threshold, harvesting must cease until the population quence of the researchers’ scarcity and the discreet habi- reaches or exceeds the threshold again. Thus, predicting tat of this viper. We conclude that the population of G. the time and numbers about when and whether snakes shedaoensis is currently at a critically low but increasing will be taken, environmental capacity (K) can be of value level; thus, population viability of the species in a long in reducing the risk of over harvest by reasonable utiliza- period appears possible. Overall, our analyses provide tion to avoid wastage. both a cautionary tale and encouragement for conserva- Inbreeding depression Inbreeding depression should tion biologists who use census data and model to estimate also be integrated in demographic risk assessment and population size and endangered status of their study or- important effects of inbreeding depression may be con- ganisms. Moreover, in the study of snake status, we iden- cealed. If the ditch on the island can act as significant tified the Shedao pit-viper among the priorities for con- barriers to gene flow, which can ultimately reduce the servation. overall genetic diversity of populations and not increase the risk for extinction. So it is therefore important that 5.6 Management implications On the one hand, fluc- studies incorporate gene flow and diversity of the sub- tuations of the environment interfere with the island eco- populations of G. shedaoensis on the island to make ac- systems. On the other, they lose their genetic diversity curate predictions about the impacts of inbreeding de- due to limited dispersal. Correct handling of the relation- pression on populations. ships between people, snakes and birds, the relations be- Environmental capacity decreasing Although the tween protection and economic development, intensi- fying research and effective management, and raising the habitat on the island is broadly homogeneous, subtle spa- public’s awareness of protection are effective ways of tial variation in aspects such as slope, elevation, and protecting the G. shedaoensis population and restoring its vegetation cover undoubtedly influence factors such as resources. 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 in- 6. Conclusions creasing in future. The loss of many animal species throughout the world is 5.4 Testing and using the model Clearly, estimates of inevitable and apparently unavoidable. In other instances, such parameters can be substantially affected by habitat perpetuation of a species can be achieved only by expen- conditions and population status. Although the validity of diture of a prohibitively large sum of money. In view of this model has been verified for G. shedaoensis on the the Shedao pit-viper’s value to medicine and the apparent island, no validation has been conducted for other snakes suitability of this animal for laboratory life, it would be or larger-bodied . Hence, uncritical use of such fatuous negligence to allow this species to become ex- data, without an understanding of the criterion in which tinct when so little is required to ensure its survival. census conditions affect parameter estimates, can lead to The existing management measures set by the nature serious error. 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