Demographic Evidence of Illegal Harvesting of an Endangered Asian Turtle

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1 Contributed Paper Demographic Evidence of Illegal Harvesting of an Endangered Asian Turtle YIK-HEI SUNG, NANCY E. KARRAKER, AND BILLY C. H. HAU School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China Abstract: Harvesting pressure on Asian freshwater turtles is severe, and dramatic population declines of these turtles are being driven by unsustainable collection for food markets, pet trade, and traditional Chinese medicine. Populations of big-headed turtle (Platysternon megacephalum) have declined substantially across its distribution, particularly in China, because of overcollection. To understand the effects of chronic harvesting pressure on big-headed turtle populations, we examined the effects of illegal harvesting on the demography of populations in Hong Kong, where some populations still exist. We used mark-recapture methods to compare demographic characteristics between sites with harvesting histories and one site in a fully protected area. Sites with a history of illegal turtle harvesting were characterized by the absence of large adults and skewed ratios of juveniles to adults, which may have negative implications for the long-term viability of populations. These sites also had lower densities of adults and smaller adult body sizes than the protected site. Given that populations throughout most of the species range are heavily harvested and individuals are increasingly difficult to find in mainland China, the illegal collection of turtles from populations in Hong Kong may increase over time. Long-term monitoring of populations is essential to track effects of illegal collection, and increased patrolling is needed to help control illegal harvesting of populations, particularly in national parks. Because few, if any, other completely protected populations remain in the region, our data on an unharvested population of big-headed turtles serve as an important reference for assessing the negative consequences of harvesting on populations of stream turtles. Keywords: big-headed turtle, China, overcollection, overexploitation, Platysternon megacephalum Evidencia Demográfica de la Captura Ilegal de una Tortuga Asiática en Peligro Resumen: La presión de captura sobre tortugas dulceacuícolas asiáticas es severa, y las declinaciones poblacionales dramáticas de estas tortugas se deben a la colecta no sustentable para mercados de alimento, comercio de mascotas y la medicina tradicional china. Las poblaciones de Platysternon megacephalum han declinado sustancialmenteen toda suárea de distribución, particularmente en China, debido a la sobrecolecta. Para entender los efectos de la presión de captura crónica sobre las poblaciones de P. megacephalum, examinamos los efectos de la captura ilegal sobre la demografía de poblaciones en Hong Kong, dondetodavía existen algunas poblaciones. Utilizamos métodos de marca-recaptura para comparar las características demográficas entre sitios con historia de captura y un sitio en un área completamente protegida. Los sitios con una historia de captura ilegal de tortugas se caracterizaron por la ausencia de adultos grandes y proporciones de juveniles adultos sesgadas, lo que puede tener implicaciones negativas para la viabilidad a largo plazo de las poblaciones. Estos sitios también tuvieron menor densidad de adultos y menor tamaño corporal de adultos que en el sitio protegido. Debido a que las poblaciones en la mayor parte del área de distribución de la especie son cosechadas intensivamentey cada vez es más difícil encontrar individuos en China continental, la captura ilegal de tortugas de poblaciones en Hong Kong puede incrementar en el futuro. El monitoreo a largo plazo de las poblaciones es esencial para rastrear los efectos de la colecta ilegal, y se requiere de mayor patrullaje para ayudar a controlar la cosecha ilegal de poblaciones, particularmente en los parques nacionales. Debido Current address: Kadoorie Conservation China, Kadoorie Farm and Botanic Garden, Lam Kam Road, Tai Po, New Territories, Hong Kong SAR, China, heisyh@gmail.com Current address: Department of Natural Resources Science, University of Rhode Island, Kingston, RI 02881, U.S.A. Paper submitted October 22, 2012; revised manuscript accepted March 9, , Volume00,No.0,1 8 C 2013 Society for DOI: /cobi.12102

2 2 Effects of Harvesting on Turtles a que en la región permanecen pocas, si acaso alguna, poblaciones completamente protegidas, nuestros datos de una población no cosechada de P. megacephalum son una referencia importante para la evaluación de las consecuencias negativas de la cosecha de poblaciones de esta especie. Palabras Clave: China, Platysternon megacephalum, sobrecolecta, sobreexplotación Introduction Harvesting is broadly recognized as one of the major threats to wild vertebrate populations (Bennett et al. 2002; Yiming & Wilcove 2005; Hoffmann et al. 2010). This threat has increased in recent decades as human populations and the demand for wild-caught animals have grown. Species that are heavily harvested suffer from a broad array of demographic (Milner et al. 2006) and distributional effects (Bodmer et al. 2002; Corlett 2007), including shifts in population sex ratios associated with sex-biased harvesting (Ginsberg & Milner-Gulland 1994), reduced fecundity (Milner-Gulland et al. 2003), and declines in abundance (Tomillo et al. 2008). These effects vary in geographic scope. Increases in villager numbers engaged in subsistence harvesting have led to local population declines (Fa et al. 2002), and heavy, persistent regional demand has resulted in the functional or ecological (Estes et al. 1989) extinction of species in the wild (Redford 1992). Understanding the effects of harvesting on wildlife populations is crucial for conservation and conservation-related management (Lande et al. 1997). However, there have been relatively few studies in which the effects of harvesting on a taxonomic group have been quantified (John & Brown 2009), particularly for small vertebrates such as turtles. Unsustainable harvest of Asian freshwater turtles for food markets, traditional Chinese medicine, and pet markets have contributed to the Asian turtle crisis (Cheung & Dudgeon 2006). As much as 80% of freshwater turtles are threatened to some degree, and over 50% are listed as endangered or critically endangered (IUCN 2012). These percentages are higher than those for mammals, birds, and amphibians (Buhlmann et al. 2009). Population sizes of most Asian turtle species have been small for so many decades that studies on their ecology have been nearly impossible (Shen et al. 2010). A confounding factor is that chronic overharvesting drives up market prices as individuals become scarcer, making remaining turtles more valuable to collectors (Eisemberg et al. 2011). Despite years of chronic pressure on turtle populations to supply food, medicine, and the pet trade, understanding of the demographic consequences of harvesting on populations is lacking. Turtles are long-lived animals and 3 aspects of their life histories render them vulnerable to human exploitation (Iverson 1982). Many species of turtles do not reach sexual maturity until years of age, and heavy collection may result in populations containing few reproductively active individuals. Clutch sizes of many species are low and mortality of eggs can be high, resulting in low recruitment each year (Congdon et al. 1993). Many species show sexual size dimorphism (Berry & Shine 1980) (females larger than males). Harvesting of turtles for food markets and traditional Chinese medicine may initially target the largest individuals, which are often females, and therefore affect recruitment. In addition, targeting females for collection can lead to skewed sex ratios, making it difficult for individuals to find mates. Thus, the ability of turtle populations to adapt to anthropogenic threats in their environment is limited (Congdon et al. 1993; Heppell 1998). Studying the effects of overharvesting on turtles is difficult because of the challenges of finding unharvested populations to serve as references. In addition, long-term data are most often not available for evaluating trends in harvested populations. A few researchers have examined the effects of harvesting on turtle populations in North America (Close & Seigel 1997; Gamble & Simons 2004; Brown et al. 2011), Australia (Fordham et al. 2007), and Papua New Guinea (Eisemberg et al. 2011). However, there has been no quantitative study on the effects of harvesting on any Asian freshwater turtles. Five species of freshwater turtles are native to Hong Kong (Karsen et al. 1998), but numbers of all but one species, the big-headed turtle (Platysternon megacephalum), are so low that they are rarely encountered in the wild. Big-headed turtles inhabit upland, rocky, and fast-flowing streams (Ernst & Barbour 1989) in China, Thailand, Vietnam, Cambodia, Laos, and Myanmar. Although currently listed as endangered by the International Union for the Conservation of Nature (IUCN 2012), present in CITES Appendix II (CITES 2011), and protected by law in China and Hong Kong, big-headed turtles are still captured and commonly appear in food and pet markets throughout the region (Shi et al. 2004; Cheung & Dudgeon 2006; Zhou & Jiang 2008). Some commercial turtle farms claim to breed this species successfully in captivity, although it is widely known that this species does not reproduce readily in captivity Turtle farms label wild-caught big-headed turtles as captive-bred individuals so they can sell them in the open market (Shi et al. 2007). Efforts to collect big-headed turtles for study in South China have yielded few individuals. In 2 studies, only 16 individuals were caught in over 4000 trapping days (Gong et al. 2006; Wang et al. 2010). In addition to decreasing numbers of individuals entering the market, it is evident that populations of big-headed turtles have been heavily depleted and populations are in drastic decline in China (Lau & Shi 2000). In other countries within

3 Sung et al. 3 its distribution, including Laos, Vietnam, and Cambodia, population sizes are likely to be low because of high pressure from illegal collection and limited habitats (Hendrie 2000; Stuart & Timmins 2000; Tana et al. 2000). The species was recently proposed for upgrading on the IUCN Red List from endangered to critically endangered to highlight the immediate need to conserve this species (Horne et al. 2012). In addition, the scarcity of big-headed turtles throughout much of its range continues to limit understanding of its ecology (Shen et al. 2010). Despite ongoing harvesting pressure on big-headed turtle populations, individuals can still be found in some streams in Hong Kong (Lau et al. 2000), including at one site that is completely protected. Given the acute nature of the Asian turtle crisis (van Dijk et al. 2000), remaining populations of turtles in this region provide a rare opportunity to study the ways in which overharvesting affects populations. Our objective was to examine the effects of illegal harvesting on population size, age class structure, and sex ratio of big-headed turtles. Methods Study Area We conducted this study in 5 streams in Hong Kong Special Administrative Region, China ( N, E): 4 streams in national parks and 1 stream in a private conservation area. Information on illegal harvesting activities in these streams was documented by interviewing ecologists and researchers and through our own observations. We classified the 4 sites in national parks as harvested sites because illegal turtle traps were found at each site on multiple occasions. Although we could not obtain quantitative information on past harvesting frequency and effort, illegal turtle harvesting likely intensified in frequency and extent in Hong Kong since approximately1998 because before 1998 turtle traps had not been found in these streams by ecologists who occasionally visited the streams (M. W. N. Lau, personal communication). To ensure the safety of the turtle populations we studied, we have not disclosed the exact locations of our study sites. Study streams were at least 1 km apart. The streams where harvesting occurred (hereafter harvested sites) are referred to as MS, SH, TO, and TN, and the protected area (hereafter unharvested site) is referred to as KFBG. The KFBG site is a private reserve with open access to the public during the daytime. The reserve is fenced and frequently patrolled both day and night to ensure that no unpermitted entry occurs. Traps have never been found in streams in the reserve, and trespassers collecting turtles have never been observed during frequent visits by researchers and other KFBG personnel, including security. Thus, we assumed it has been an unharvested site since its establishment in In South China, as throughout Southeast Asia, it is rare to find a study site for which it can be established that no harvesting has occurred. We believe KFBG is one of very few unharvested streams in the region and possibly the only one in South China. Turtle Sampling From September 2009 to June 2011, we conducted mark-recapture surveys in the harvested and unharvested streams. We used hoop traps and visual encounter surveys to survey for big-headed turtles along stream sections that ranged from 200 to 680 m. Differences in lengths of stream reaches surveyed were related to availability of habitat in streams and safety concerns associated with extremely steep sections of streams. In an early phase of the study, we conducted 32 visual encounter surveys at KFBG and 19 surveys at MS. We surveyed at night between 19:00 and 23:00. Two observers walked upstream while scanning the stream with headlamps and probing beneath stones for turtles. At all sites, we deployed hoop traps baited with dead fish in late afternoon or early evening and checked them later the same night or the following morning. We set traps each trapping night, depending on the length of the reach being sampled, and set traps in each stream 7 11 times. We conducted 51 visual encounter surveys for a total of 263 hours and 43 trapping sessions (5124 trap hours). We collected basic morphometric data on captured turtles, including straight-line carapace length and plastron length, measured with dial calipers, and body mass, measured with spring scale. We used marginal scale notching to mark turtles and followed a numbering system developed by Cagle (1939) that allowed us to recognize individuals. The age at which big-headed turtles reach sexual maturity in the wild is unknown. By examining the secondary sexual characteristics, including distance of cloaca from the edge of the plastron and thickness of the tail base above the cloaca, we were able to sex all individuals with plastron length >89 mm; thus, we considered all individuals of <89 mm juveniles. Data Analyses We compared mean body sizes (plastron length) of turtles between sexes and between harvested and unharvested sites with a 2-way analysis of variance (Zar 1999). We combined the data for the 4 sites where illegal harvesting has occurred because of the small sample sizes in some sites. We divided the plastron lengths of individuals captured at all sites into 10-mm size classes from 20.0 to mm and examined the difference in population structure between the unharvested site and harvested sites. To examine differences in sex ratio and age class structure (proportion of juveniles to adults), we

4 4 Effects of Harvesting on Turtles Table 1. Mean of straight-line carapace length, straight-line plastron length, and body mass for female, male, and juvenile big-headed turtles (Platysternon megacephalum)inhongkong. Measurement Female (SE, range) Male (SE, range) Juvenile (SE, range) Carapace length (mm) (2.1, ) (3.7, ) 67.0 (2.2, ) Plastron length (mm) (1.8, ) (2.9, ) 55.0 (2.1, ) Body mass (g) 323 (18, ) 573 (29, ) 80 (7, 8 273) Sample size Figure 1. Size class distributions of big-headed turtles (Platysternon megacephalum) capturedfrom1 unharvested site and 4 harvested sites in Hong Kong. conducted pairwise comparisons between the unharvested site and each of the harvested sites with Fisher s exact test (Zar 1999). Normality and homogeneity were tested before parametric statistics were used. Transformations of response variables were made if assumptions of normality or homogeneity were violated. We conducted all analyses in SPSS 16 (SPSS, Chicago, Illinois). Differences were considered significant at α = We used the Jolly-Seber open-population model (POPAN) in Program MARK to estimate population sizes for each stream (White & Burnham 1999). Population densities were calculated by dividing estimated population sizes by the length of the study stream. Results We made 261 captures of 138 individuals, of which 26 were males, 30 were females, and 82 were juveniles. Recapture rate was 47%. The overall sex ratio was 1:1.2, which was slightly female biased but not significantly so (χ 2 = 0.010, p = 0.92). For all turtles captured, mean carapace length was mm (SE 3.1), mean plastron length was 82.8 mm (SE 2.6), and mean weight was 226 g(se= 19.9) (Table 1). The major difference in plastron-length classes among the sites was the absence of individuals with plastron length >110 mm in harvested sites (Fig. 1). Body sizes differed significantly between males and females (F 1,52 = 23.34, p < 0.001) and harvested and unharvested sites (F 1,52 = 46.56, p < 0.001) (Table 2). Males were significantly larger than females at the unharvested site than at the harvested sites. The interaction between sexes and harvested and unharvested sites was significant (F 1,52 = 7.73, p < 0.008). In a follow-up 1-way analysis of variance, males at unharvested sites were the largest individuals overall (p < in all cases), females at unharvested sites were larger than females at harvested sites (p = 0.034), and males at harvested sites were similar in size to females at both unharvested sites (p = 0.555) and harvested sites (p = 0.533). Estimated population density of males was highest at the unharvested site, KFBG. Estimated density of females in KFBG was higher than all harvested sites except SH (Fig. 2). Population density of juveniles was lowest at the unharvested site. Sex ratios did not differ from 1:1 at any of the sites (KFBG: χ 2 = 0.13, df = 1, p = 0.72; MS: χ 2 = 0, df = 1, p = 1.00; SH: χ 2 = 0.4, df = 1, p = 0.53; TO: χ 2 = 0.5, df = 1, p = 0.48; TN: χ 2 = 0.67, df = 1, p = 0.41) (Table 3). Sex ratios of turtles captured in unharvested and harvested sites were similar, but percentages of juveniles differed (Table 3). The percentage of juveniles in KFBG was significantly higher than at all harvested sites. Discussion We detected several demographic signals in the harvested sites that are indicative of ongoing negative effects to populations caused by illegal harvesting that may affect the long-term viability of these populations. No adults with plastron lengths >110 mm were captured in harvested sites, whereas the plastron lengths of over 30% of

5 Sung et al. 5 Table 2. Mean plastron length (mm) of juvenile, female, and male big-headed turtles (Platysternon megacephalum)fromthe5studysitesinhong Kong. Site Juveniles (SE, n) Females (SE, n) Males (SE, n) KFBG a (4.31, 14) (2.74, 16) (2.53, 14) MS (4.37, 14) 95 (1) b 91 (1) b SH (4.57, 16) (2.14, 6) (4.41, 4) TO (4.92, 17) (4.25, 3) (1.52, 5) TN (2.82, 21) (3.14, 4) (7.90, 2) a Unharvested site. b Sample size <2, so SD could not be calculated. Figure 2. Estimated population density of juvenile, female, and male big-headed turtles (Platysternon megacephalum) captured at the 5 study sites in Hong Kong from September 2009 to June 2011 (KFBG, unharvested site). Table 3. Sex ratio and proportions of juvenile big-headed turtles (Platysternon megacephalum) capturedatthe5studysitesinhong Kong. Sample Sex ratio Juveniles Site a size (M:F) p (%) p KFBG 44 1 : 1.15 na 31.8 na MS 16 1 : <0.001 SH 26 1 : TO 27 1 : TN 25 1 : <0.001 a The KFBG site is the unharvested site. We conducted pairwise comparisons between the unharvested site and each of the harvested sites. individuals captured in the unharvested site were >110 mm, including females as large as 127 mm and males as large as 138 mm. In a study in North America, harvesting pressure on painted turtle (Chrysemys picta)populations led to lower abundances at harvested sites, and some collectors reported preferring larger adults because they are more valuable in food markets (Gamble & Simons 2004). However, we suspect our results are unlikely to be related to the preference for larger turtles by illegal collectors. For big-headed turtles, small specimens are sold as pets and larger individuals are sold in food, Chinese traditional medicine, and pet markets (Chen et al. 2009). On the basis of our observations, trappers normally place rectangular wire-mesh traps in streams and check them later, and it is unlikely that there is a bias in sizes of turtles captured by trapping. Although illegal turtle trappers probably do not prefer a specific size of bigheaded turtle, larger adults are more easily detected and caught by trappers as trappers travel along the streams at night. This likely contributes to the absence of large adults in harvested sites. Moreover, larger turtles may be older and, if older, have inhabited the streams for a longer period. Thus, they would have a higher cumulative probability over time of having been caught by illegal trappers. Results of several other studies suggest that past harvesting of turtles is responsible for the absence of individuals from larger size classes. In a study on populations of red-eared sliders (Trachemys scripta elegans) in the United States, no individuals with a carapace length over 240 mm were captured from sites where harvesting occurred, whereas over 20% of individuals from protected sites were larger than 240 mm in carapace length (Close & Seigel 1997). In a study on alligator snapping turtles (Macrochelys temminckii) in the United States, large adults were scarce owing to past commercial harvesting (Riedle et al. 2008), and similar results were obtained from other populations of this species in the region (Jensen & Birkhead 2003; Shipman & Riedle 2008). We suggest that the absence of large adults in harvested sites

6 6 Effects of Harvesting on Turtles in our study was likely caused by past and probably ongoing illegal harvesting. There may be other factors involved in size distributions among streams. Absence of the larger size classes of turtles from the harvested populations may be associated with variation in the maximum attainable size among different populations. The maximum attainable size of turtles within a population is to be related to diet (Gibbons 1967), growth rate (Cagle 1946), and competition (Dunham & Gibbons 1990). To date, there have been no quantitative studies of the diet of big-headed turtles. Thus, the relation between their body sizes and diets is unknown. It has been suggested that turtles with the most rapid growth rates in a population may cease growing when their size is larger than others in the population (Gibbons 1967). Such a pattern could lead to different maximum attainable sizes in different populations. However, we found that the larger adult turtles in harvested sites continued to show significant growth between recaptures (Y.H.S., unpublished data), which may indicate that the maximum attainable sizes of these populations may be larger than the sizes of largest individuals caught. This finding may suggest that larger individuals previously existed in the harvested populations but were removed. Under this scenario, the absence of large adults in harvested sites is unlikely to be explained by competition or differential growth rate among sites. In addition to the absence of large adults, on average male and female turtles were 23% and 10% larger in the unharvested site than in harvested sites. Similarly, in a population of pig-nosed turtles (Carettochelys insculpta) in Papua New Guinea, average female body sizes decreased over 30 years because of harvesting pressure (Eisemberg et al. 2011). Smaller females produce fewer, smaller eggs, attributes indicate demographic changes that may affect recruitment. Larger adult turtles generally exhibit higher fecundity, and their offspring may have higher survival rates (Congdon & Gibbons 1985; Paitz et al. 2007). Larger sizes of adult turtles in the unharvested site in our study may have large implications for the longterm persistence and viability of the population. Adult density in the unharvested site was higher than at all harvested sites, except female density in SH, and these differences in density are likely attributable to past harvesting activities. During the course of this study, we did not detect any turtle traps at SH during our frequent visits. However, trapping had been observed at this site prior to initiation of this study, and it is possible that no trapping has occurred recently. The percentage of juveniles was lower at the unharvested site than in harvested sites. This finding is inconsistent with studies demonstrating that turtle populations affected by disturbance have reduced recruitment (Marchand & Litvaitis 2004). However, higher percentages of juveniles may not necessarily imply stable populations (Crouse & Frazer 1995); rather, it may imply a shift in age-class percentages resulting from fewer adults. For many turtle species, the number of juveniles can exceed the number of adults by times (Gibbs & Amato 2000). But this is likely not the case for bigheaded turtles, which have a mean clutch size of about 3 eggs (Y.H.S., unpublished data) and exhibits lower fecundity than most other turtle species. Percentages of juveniles in populations of yellow-margined box turtles (Cuora flavomarginata) and Chinese stripe-necked turtles (Mauremys sinensis) in Taiwan are 22% and 21%, respectively (Chen & Lue 1999, 2009), which is similar to the 32% juveniles we documented in our unharvested population. We conclude that the high percentages of juveniles observed in harvested sites, ranging from 63% to 88%, may be explained by the removal of adults by collectors. Hong Kong has a long history of forest loss. The region underwent nearly complete deforestation before World War II (Corlett 1999) and was associated with local extinction of many forest-dependent mammals and birds (Hau et al. 2005). The high densities of turtles we found demonstrate that big-headed turtles are relatively resilient to deforestation because they have survived in streams with highly degraded riparian vegetation that sometimes includes shrubs (Y.H.S., personal observation). On the basis of these observations, our results further suggest that human exploitation has probably been the most important factor responsible for the severe declines of populations of big-headed turtles in South China. Although the inferences that can be made on the basis of our results are limited by the low number of unharvested sites, our study provides important baseline data on a big-headed turtle population that has not been affected by harvesting, a situation that is extremely rare and valuable in Southeast Asia. In contrast to the unharvested population in this study, other big-headed turtle populations in South China have declined substantially (Stuart & Timmins 2000; Gong et al. 2006), and we speculate that most populations are too small to be self-sustaining over the long term, particularly those that are harvested. Harvest of big-headed turtles is probably lower in Hong Kong than in other parts of its range because of the relatively high living standard in Hong Kong. However, we are highly concerned that harvesting of big-headed turtles in Hong Kong will increase in the near future to meet the demand of the food and pet markets in mainland China and throughout Southeast Asia. We recommend stronger protection against illegal turtle harvesting to safeguard the populations that remain in the wild. Given the limitation of resources for enforcement of wildlife regulations, we suggest enforcement personnel identify a number of key areas for big-headed turtles, for example unprotected streams included in this study, and patrol for illegal turtle traps regularly to protect what are probably some of the most robust remaining populations of big-headed turtles.

7 Sung et al. 7 Acknowledgments We thank the staff of Kadoorie Farm and Botanic Garden for logistic and technical assistance and particularly A. Brown, M. Lau, G. Ades, and P. Crow for project support and helpful discussion. We are grateful to many students from the University of Hong Kong and other volunteers for their help in the field. All procedures were approved by the Committee on the Use of Live Animals in Teaching and Research, the University of Hong Kong (CULATR ). Literature Cited Bennett, E. L., E. J. Milner-Gulland, M. Bakarr, H. E. Eves, J. G. Robinson, and D. S. Wilkie Hunting the world s wildlife to extinction. Oryx 36: Berry, J. F., and R. Shine Sexual size dimorphism and sexual selection in turtles (order Testudines). Oecologia 44: Bodmer, R. E., J. F. Eisenberg, and K. H. Redford Hunting and the likelihood of extinction of Amazonian mammals. Conservation Biology 11: Brown, D. J., V. R. Farallo, J. R. Dixon, J. T. Baccus, T. R. Simpson, and M. R. J. 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