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A Recent Harvest Monitoring of Cuora amboinensis in Sumatra and Kalimantan
Muhammad Alif Fauzi
1*, Awal Riyanto
2, Amir Hamidy
2, Nia Kurniawan
11Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Brawijaya, Malang, Indonesia
2Museum Zoologicum Bogoriense, Research Center for Biology- The Indonesian Institute of Sciences (LIPI), Widyasatwaloka Building, Jl. Raya Jakarta Bogor Km46 Cibinong 16911, Indonesia
Abstract
Harvest monitoring is an alternative strategy to determine the impacts of exploitation which is useful for conservation strategies. One of the exploited turtles, C. amboinensis in three Indonesia provinces that have high rates of turtle harvesting, North Sumatra, South Sumatra, and Central Kalimantan were moniotored and reported here. The harvest monitoring was carried out by measuring harvested specimens based on three characters comprising median carapace length (MeCL), maximum carapace width (MaCW), and biomass of turtle (Wt). The collected data were compared with the previous monitoring in 2006. This study showed that the harvested size turtle was relatively similar to that of 2006 monitoring, in North Sumatra and Central Kalimantan. Furthermore, in North Sumatra, bigger individuals and larger quantities of the juvenile were recorded whereas in Central Kalimantan the harvest characteristics showed a similar pattern compared to previous monitoring. The female individuals were dominantly harvested in all locations, with detailed sex ratio male: female 1:1.7 (North Sumatra), 1:1.6 (South Sumatra), and 1:1.1 (Central Kalimantan). In the current monitoring, there was no evidence of a decline in harvest size that might indicate that the harvest activities of C.amboinensis in Indonesia are not yet detrimental to the wild populations. However, to reveal the sustainable harvest of this species in the future, long-term monitoring and intense supervision are needed.
Keywords: Cuora amboinensis, harvest size, monitoring
INTRODUCTION
Currently, the wildlife trade has developed as big businesses that threaten biodiversity [1,2,3]. These activities will continue to grow in several countries depending on the high-demand market, population growth, and economic growth [1,4]. Wildlife trade will affect species decline [5], change of behavior [6], biodiversity decline [7], and diseases [8]. Wildlife trade activities are regulated in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) with 183 countries as parties. CITES plays a role in regulating and ensure that the plants and animals trade does not decline and extinction in the wild. CITES classified animals and plant into three categories, appendices I, II, and III based on the threat level in International trade. All parties should be reports annually of trading activities to the CITES
Correspondence address:
Muhammad Alif Fauzi
Email : [email protected] Address: Department of Biology, Faculty of
Mathematics and Natural Sciences, Universitas Brawijaya, Malang, Indonesia
secretariat which has been regulated in article VIII CITES [9]. Although the legal trade is regulated by CITES, the illegal wildlife trade still occurs [5,10]. Among vertebrate groups, turtles are the most threatened taxa [11].
Turtles are one of the most threatened vertebrate groups, which over 50% of the 356 recognized species are categorized as Critically Endangered (CR), Endangered (EN), and Vulnerable (VU) [12]. Its situation is the impact of harvesting for pets and food, habitat degradation, and loss [13]. In the Asia region, turtles are intensively harvested for traditional Chinese medicine (TCM), food, and pets [14,15,16]. Compare to the geographic region, Asia turtle species has the highest proportion of threatened which of 88 species 75% categorized are CR+EN and 83% are CR+EN+VU [17]. Among the Geoemydidae Family in Asia, Cuora amboinensis is one of the species that have a high rate level of threat [18]. Its evidence by the rapid revision of conservation status during twenty-four years (1996-2020) from near threatened (NT) to endangered (EN) [19]. C.
amboinensis are widely distributed in Southeast Asia. These species have been included in Appendices II since 2000. After listed in Appendices II CITES the total of specimens traded
41 of C.amboinensis from the wild is 755495
individuals during seventeen years (2000-2017) which is Indonesia is the main exporter of C.
amboinensis [20]. According to article IV of CITES, the principle of wildlife trade that inclusion in appendices II is regulated by a quota system. In the quota system, each parties, especially a scientific authority need to make non- detrimental findings based on biological information data to explain that trade at a safe level and does not disturb the wild population [9,21,22].
Biologically, most turtle species have a slow reproductive ability that impacts delayed population recovery. Long-term overexploitation turtles have an impact on the declining population [23,24], unbalanced sex ratio [25], and shift of size distributions [26]. The challenging on the wildlife trade is identifying the sustainability of harvest level [27]. To answer this, it is necessary to conduct studies of the harvested species at the population level or monitoring harvest. In this paper, a recent harvest monitoring of C.amboinensis in the three province which are the hub of turtle trade in Indoensia were reported .
MATERIAL AND METHOD Data Collection
This research were conducted from April to July 2019. The collection data were obtained by surveyed middlemen in Sampit (Central Kalimantan), Palembang (South Sumatra), Asahan district, Tanjung Balai (North Sumatra) and the biggest exporter in Medan (North Sumatra). The harvested size data were obtained by measurements of three morphological character of C.amboinensis according to Schoppe [28] and Riyanto & Mumpuni [22]. Sex was determined based on the plastron shape of each individual [29]. Male individuals have concave plastrons and females have plastrons relatively
flat [21]. Small individuals which did not show sexual dimorphism will be categorized as a juvenile. The distribution of subspecies were applied to determine C.amboinensis subspecies which Sumatran population as C.a. couro and Bornean population as C.a. kamaroma [12].
Measurements were taken with the 300 mm caliper and Mitutoyo digital caliper.
Measurement character included: 1) Median carapace Length (MeCL; straight-line carapace measurement taken from nuchal to supracaudal), 2) Maximum carapace width (MaCW; greatest width from left marginal to right side marginal), (Figure 1), 3) Weight (Wt; the biomass of turtle weight obtained by a digital electronic scale with the accuracy 1 gram). The data will be described quantitavely.
Figure 1. Measured character in C. amboinensis
Data Analysis
According to Schoppe [28], C.amboinensis are classified on three age classes which <116 mm as a juvenile, <160 mm as subadult, and >160 mm as an adult. The collected data were categorized in 10 mm size class interval then compared with the previous study. The compared data visualization in histogram. Data collected was used for the estimation of statistical description (mean, standard deviation, minimum, maximum).
Character
Male Female Unsex & Juv
NS (n=152) SS (n=43) CB (n=122) NS (n=266) SS (n=70) CB (n=141) NS (n=68) MeCL (mm) 183.08±20.18 195,95±10,51 186.49±13.87 170.30 ± 26.61 190.84±12.8 178.91 ±17.2 112.30±11.38
(119.80-228.20) (178.80-219.60) (127.20-209.60) (113.81-229.75) (137.11-222.45) (120.50-209.70) (88.98-132.87) MaCW
(mm) 131.98 ±10.50 136,77±6,7 130.13 ±8.39 129.11±15.69 138.20 ± 8.99 131.42±11.14 (91.87±8.66) (97.71-154.70) (121.72-148.49) (97.55-149.55) (85.28-167.26) (114.36-183.23) (94.45-155.80 76.43-114.78 Wt (gr) 909.25±242.65 983.79 ±128.06 909.36 ±172.01 849.41±374.72 1035.92±229.76 940.34±231.86 238.91±76.08 (261-1467) (716-1272) (335-1257) (113-2090) (443-1942) (301-1416) (123-413)
Table 1. Measurement of three morphological characters in males, females and juveniles of harvested C.amboinensis. Data are shown including of mean and standart deviation, followed by the range in parentheses
42
RESULT AND DISCUSSION
Harvest Characteristics
Total specimens examined were 862 individuals with details 263 individuals of C.a kamaroma and 599 individuals of C.a.
couro. Based on the age characteristics, harvests in three locations were dominated by adult individuals. In North Sumatra, the harvest trend comprises 63 % of adults, 28 % of subadults, and 9 % of juveniles. Harvest in Palembang was dominated by adult specimens (98%). In line with that, the harvest trend in middleman on Sampit comprises 90 % of adults and is followed by 10 % of subadults (Figure 2). Three age classes were recorded in North Sumatra which indicated that harvested C.amboinensis showed real condition of wild population. Its condition may be due to depend on market demand.
Figure 2. Harvested characteristic based on age class
In turtle harvest, all sizes of turtles have a market value for trading, small individuare sold as pets, but largest individuals turtles are the main target because they are more valuable in the food market [25,26]. In North Sumatra, the juvenile of C.amboinensis were traded for pets and religious ceremonies. For religious ceremony, the juvenile C.amboinensis were marked by paint on the carapace and release after finished it. In this study, some marked specimens were cauaght by hunter and middleman. The adult specimens were recorded to supply the consumption market. The harvest size in North Sumatra is similar to that of reported by Riyanto & Mumpuni [21] in which the harvested specimens were mostly dominated by subadult and adult individuals.
Of the three locations, the largest specimens was recorded from North Sumatra with MeCL character measured of 229 mm and
weight 2090 gram (Table 1). The harvest size of adult specimens in North Sumatra was dominated by 190 mm, 180 mm, and 170 mm. In South Sumatra and Central Kalimantan, the harvested C.amboinensis from both locations were dominated by 180 mm (Figure 3). In North Sumatra, large quantities of juvenile individuals were recorded which is dominated by 110 mm in size. Surprisingly, 5 biggest specimens were also recorded specimens which have reaching up to 220 mm. Comparing to previous research, the harvested C.amboinensis from North Sumatra was bigger than that of thirteen years ago (Figure 4). Its evidence by the presence of a size class of more than >200 mm. The harvested size in Central Kalimantan compare to Schoppe (2009) in their trade surveys in all parts of Kalimantan (West Kalimantan, East Kalimantan, and South Kalimantan) showed the same pattern which dominated by 180 mm in size. These results indicate that the harvest activities does not yet impact the wild population.
Figure 3. Harvested size of C.amboinensis in the three provinces
In recent monitoring shows that there is no decrease in harvest size compared to that of thirteen years ago, as monitored by Schoppe in 2006. Moreover the harvest size observed in North Sumatra is bigger. The larger size is recorded in our recent monitoring may be influenced by diet and growth rate [30].
Furthermore, the dynamics of the harvested population allow shifted to large harvest size because the resources are greater. When individuals in the population are harvested, the population will decrease and population growth will increase. The greater amount of resources available in the natural population can be utilized for growth and reproduction [31]. The critical point is knowing the optimal level of removed
43 individuals in the population to maximize the
population growth.
Figure 4. Comparison harvested size of C.amboinensis in North Sumatra
Although the decrease in the size of the harvested Amboina Box Turtles does not occur, harvesting activities that ignored the regulation and biological information can cause unsustainable harvesting. Harvesting individual with MeCL character <160 mm in large quantity is an important concern because these sizes represent individuals that have not yet reproduce and have not yet contributed to populations in the wild. However, harvest in adults female specifically targeted for commercial harvesting will affect the reduction of population and fecundity [32]. Long-term harvesting potentially affects the decline of turtles in population, it is important to consider the best management of harvest activities. Indonesia has C.amboinensis harvest regulation that prohibited pregnant individuals. This regulation should be socialized to hunters, middlemen, and exporters to prevent hunting in reproductive season [33].
Figure 5. Comparison of harvested size of C.amboinensis in Kalimantan.
Sex Ratio
Another important parameter to determine the impact of harvesting is the sex ratio [29]. In this study, sex ratios from three locations tended to be more female individuals. In North Sumatra, the sex ratio of males and females from 418 individuals is 1:1.7. Sex ratio from 113 specimens harvested in Palembang is 1:1.6. Total turtles measured in Sampit were 263 individuals with a sex ratio that almost balanced, 1:1.1. The female- biased has also occurs in Big-headed turtles both of harvested and unharvested sites [30]. The female-biased sex ratio in the population can be influenced by the different levels of age maturity between females and males. When males mature much faster than females, calculations of sex ratio in population tended to male cohorts [34].
Another reason the female-biased sex ratio can be influenced by adult male individuals as the main target for harvest.
Several studies showed the variations of unbalanced sex ratios. According to Schoppe [18], the sex ratio of C. amboinensis in the Malaysia population showed that the male and female ratio was 1:3. Schoppe [28] also monitored in Kota Bangun (East Kalimantan), the ratio of male and female was 1:1.03. Female biased sex ratio also occurred in the study population of Macrochelys temmincki with a female to male ratio of 6: 1 [26]. The unbalanced sex ratio is caused by several factors such as home range sizes, trap types of equipment, habitat preference, mortality rates, behavior [34], movement rates between sex, nest temperature [35], and overexploitation [36]. In the case of C. amboinensis, the unbalance sex ratio of wild-harvested individuals can not be justified as the impact of overexploitation because of behavior species and putting the traps in potential habitat. The males of C.amboinensis have widely home range that makes them rare to be caught. On the other hand, the female has a limited home range and the behavior tends to move slowly, which makes the female easier to be found (Aini et al. in prep).
Ecologically, it is caused by the behavior of species and food sources.
44
Table 2. Reproducrtive condition of C.amboinensis
Cuora amboinensis is the most common turtle and is abundant in several areas in Indonesia [19, 28]. It can adapt well to natural and human-modified habitats such as forests, shallow lakes, peat swamps, oil palm plantations, and rice fields [37]. The ability to adapt in unusual condition is important factor of C.amboinensis to survivorship even harvest activity still occurs and ongoing habitat loss. The adaptive C.amboinensis in various habitats is similar to the eastern long-necked turtle, Chelodina longicollis in Australia. These species persist in urban landscape habitat [38].
The adaptive activity of resilient turtles is caused by several factors such as feeding behavior in many types of food sources and the ability to respond the environmental change. The wide habitat preference of C.amboinensis makes them easy to catch. The adaptive behavior will be threatened because people community around the forest incidentally caught C.amboinensis from the oil palm plantation habitat and sell them [18,33]. Subsequently, the population study to reveal the C.amboinensis density was conducted by Riyanto & Mumpuni [22] who surveyed in oil palm plantation on North Sumatra and found that the abundance of C.amboinensis was 80 ind/
ha. These results were higher than the population in Rawa Aopa Watumohai National park with a population density of 60 ind/ha.
Recommendations
In this study, the examining of reproductive condition was conducted to determining the size limit of an immature shift to a mature individual.
Seven individuals of C. amboinensis were examined. Five male specimens over 170 mm of MeCL character showed mature individuals which have convoluted of vas deferens. The female turtle that has 174 mm of MeCL character showed that it had already reproduced with the characteristic of the presence of corpus luteum/albicans and thicked of oviduct. It indicates that the female with MeCL size 174 mm has reproduced previously. On the other hand, a
female that has MeCL 144 mm showed an immature individual which has the characteristic of absence of corpus luteum/albicans and clear of oviduct condition. (Table 2).
The limitation of harvest subadult individuals is reasonable because the reproduction value is low [39]. Although the removal of adult individuals is high risk [40] and it will impact population recovery [23]. In turtles, every stage of life history is important. A harvest strategy with egg as a target is a step towards achieving sustainable harvest for turtles [41,42].
The harvest of eggs is feasible because has a lower impact on the wild population.
Unfortunately, from the economic perspective, the utilization and feasibility of harvesting eggs are still lacking. The alternative strategy to reduce harvest from the wild is turtle farming.
These activities are not economically viable because many turtles have low survival rates and long reach maturity [16]. A harvest policy strategy that takes the biological information and economic perspective of the community that depends on harvesting activities is urgently needed. If the management of species is carried out consistently by strong supervision, it is likely to increase the population of exploited turtles [42].
To ensure sustainable harvesting, firstly we need to know the impact of harvest activities.
However, the studies on harvesting effects in the population are very difficult to detect because of the limitations of the ecological factor in certain regions [43]. Determining the effect of commercial harvesting turtles cannot be detected in the short term monitoring [21] which requires a review of survivorship aspects and the ability to mature individuals.
According the natural history of C.amboinensis, the reproductive ability is laying eggs one to three eggs every month in the breeding season [44]. Maturity from juvenile to adult takes 5,5-6 years [28]. In an ecosystem, the turtle has the ability as an agent for seed dispersal and germination. [45]. C.amboinensis is an important turtle that has an ecological role as seed dispersal and accelerates the germination of edible grains [46]. It is very important to determine sustainable harvest quotas based on the precautionary approach, regarding the ecological roles of turtles and natural history species. Many turtles are threatened because of slow reproductive capacity makes it difficult to recover populations in the wild after harvesting [47]. This condition makes all country which
45 ratified CITES, especially Indonesia, should be
appropriately quantify the turtles that harvested from the wild [23] for a sustainability goal. It is needed to set the annual quota by comprehensive research because the determined annual quotas did not consider based on scientific reason.
Considering the harvest impact of C.amboinensis does not occur, long-term monitoring is needed for the conservation strategy of the species. Although Indonesia has a harvest quota, the supervision and enforcement are lacking. Hence, it is necessary to reinforcement of regulation and strengthening supervision regularly by Management Authority to prevent illegal, over-exploitation and sharp decline population in the wild. Further investigastion on reproductive condition is urgently needed to ensure sustainable harvesting of C.amboinensis in Indonesia.
CONCLUSION
The harvest characteristics of C.amboinensis in the three Indonesian provinces were dominated by adult individuals, even though juvenile individuals were recorded in North Sumatra. The sex ratio of harvested Amboina box turtles tends to be dominated by female individuals. The harvested size of C. amboinensis in North Sumatra and Central Kalimantan did not show a decrease in harvest size compare to previous research.
ACKNOWLEDGEMENT
Authors thank all middlemen and exporters who were allowed to carry out the monitoring.
Many thanks to staffs of BBKSDA Sumatra Utara (Agency for Conservation of Natural Resources of North Sumatra), BKSDA Sumatra Selatan (Agency for Conservation of Natural Resources of South Sumatra), and BKSDA Kalimantan Tengah (Agency for Conservation of Natural Resources of Central Kalimantan) for permits and teamwork during data collection. Thank you in advance Mrs.Mumpuni, Mrs. Evy Arida, and Mr. Mulyadi which help researchers during data collection.
Thanks a lot to Daniel Natusch and Misbahul Munir for valuable discussion and comment.
Special thanks to Sabine Schoppe and Kanitha Krishnasamy for sharing data monitoring in 2006.
This research was funded by Project DIPA Pusat Penelitian Biologi LIPI 2019 “Studi dan Monitoring Tumbuhan dan Satwa Liar yang Masuk Apendiks CITES Serta Aspek Ekonomi dan
Antropologinya (34000.002.051 A). All authors contributed equally to the manuscript.
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