Diversity, Habitat Distribution, and Indigenous Hunting of Marine Turtles

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55 HOSTED BY Contents lists available at ScienceDirect 56 57 Journal of Asia-Pacific Biodiversity 58 59 60 journal homepage: http://www.elsevier.com/locate/japb 61 62 63 Original article 64 65 1 Diversity, habitat distribution, and indigenous hunting of marine 66 2 67 3 turtles in the Calamian Islands, Palawan, Republic of the Philippines 68 4 69 a,b,* b b 5 Q16 Christopher N.S. Poonian , Reynante V. Ramilo , Danica D. Lopez 70 6 a 71 7 Community Centred Conservation (C3), London, UK b C3 Philippines and Micronesia Programme, Busuanga, Philippines 72 8 73 9 74 10 article info abstract 75 11 76 12 Article history: All of the world’s seven species of marine turtle are threatened by a multitude of anthropogenic pres- 77 13 Received 26 May 2015 sures across all stages of their life history. The Calamian Islands, Palawan, Philippines provide important 78 14 Received in revised form foraging and nesting grounds for four species: green turtles (Chelonia mydas), hawksbill turtles (Eret- 79 22 December 2015 15 mochelys imbricata), loggerheads (Caretta caretta), and leatherbacks (Dermochelys coriacea). This work 80 Accepted 30 December 2015 16 aimed to assess the relative importance of turtle nesting beaches and local threats using a combination of Available online xxx 81 17 social science and ecological research approaches. Endangered green turtles and critically endangered 82 hawksbills were found to nest in the Calamianes. The most important nesting sites were located on the 18 Keywords: 83 islands off the west of Busuanga and Culion, particularly Pamalican and Galoc and along the north coast 19 Busuanga 84 20 Q1 Coron of Coron, particularly Linamodio Island. Opportunistic hunting and egg collection, conducted legally by fi 85 21 Culion indigenous communities, is the most signi cant threat to sea turtles in the area. Sites particularly vulnerable to hunting were found to be Galoc Island, Pamalican Island, and Panlaitan Island. Raising 86 22 Linacpan nesting beaches awareness, community engagement, and understanding of socio-cultural drivers of sea turtle exploita- 87 23 sea turtles tion, particularly among indigenous communities, are essential to gain support for any effective con- 88 24 Q2 Tagbanua servation program. Additionally, more effective enforcement of laws related to the trade in sea turtle 89 25 products is required to close the commercial and export markets. 90 26 Copyright Ó 2016, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). 91 27 Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// 92 28 creativecommons.org/licenses/by-nc-nd/4.0/). 93 29 94 30 95 31 96 32 97 33 Introduction stages at which they are most vulnerable. Turtles are particularly 98 34 vulnerable to human exploitation during nesting, when they are 99 35 Owing to their longevity, slow maturation rates, and complex easily accessible to coastal populations, usually for subsistence 100 36 life histories, marine turtles are highly vulnerable to a multitude of purposes (Humber et al 2014). 101 37 anthropogenic threats operating across their life-history (Wallace Marine turtle populations worldwide are in urgent need of 102 38 et al 2011). They undertake large-scale migrations, utilizing a conservation action. Globally, the number of mature females 103 39 wide range of habitats but spending the majority of their lives in nesting annually has diminished over the past three generations, by 104 40 the deep oceans. Female turtles return annually to their natal 84e97% for hawksbill turtles, Eretmochelys imbricata [listed on the 105 41 beaches to nest (Lohmann et al 2013), allowing critical areas of the International Union for the Conservation of Nature (IUCN) Red List 106 42 Q4 nesting habitat to be identified and providing a rare opportunity to as Critically Endangered; Mortimer and Donnelly 2008] and 48e 107 43 evaluate populations and their distribution to inform conservation 67% for green turtles, Chelonia mydas (listed on the IUCN Red List as 108 44 management. It is impossible to guard against all threats to a given Endangered; Seminoff 2004). All seven of the world’s species of 109 45 population of marine turtles, or to protect every area of habitat they marine turtle are included within the threatened categories of the 110 46 utilize, so conservation efforts must therefore focus on life-history IUCN Red List (IUCN 2014) and in Appendix I of the Convention on 111 47 International Trade in Endangered Species, prohibiting interna- 112 48 tional trade in these species and their products (UNEP-WCMC 113 49 2015). 114 50 Q3 * Corresponding author. Tel.: þ44 20 8144 9693. There is a severe deficiency of current scientific research on 115 51 Peer review under responsibility of National Science Museum of Korea (NSMK) and 116 Korea National Arboretum (KNA). marine turtles in the Philippines, as is the case for much of 52 117 53 http://dx.doi.org/10.1016/j.japb.2015.12.006 118 54 pISSN2287-884X eISSN2287-9544/Copyright Ó 2016, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier. 119 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Poonian CNS, et al., Diversity, habitat distribution, and indigenous hunting of marine turtles in the Calamian Islands, Palawan, Republic of the Philippines, Journal of Asia-Paciﬁc Biodiversity (2016), http://dx.doi.org/10.1016/j.japb.2015.12.006 JAPB111_proof ■ 23 January 2016 ■ 2/5

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1 Southeast Asia (Gomez 1980; Shanker and Pilcher 2003), despite The Tagbanua of the Calamianes are one of the few indigenous 66 2 the fact that the country’s waters are likely to harbor internation- tribes still practicing their traditional lifestyles in the Philippines. 67 3 ally signiﬁcant populations. To date, the majority of research in the The Philippines’ constitution guarantees the rights of indigenous 68 4 Philippines has focused on the Turtle Islands, Tawi Tawi, where over communities to their ancestral land and sea resources (Capistrano 69 5 one million C. mydas eggs are laid each year (Cruz 2002; Lejano and 2010; Capistrano and Charles 2012). Fishing, hunting, and 70

6 Q5,6 Ingram 2007; Trono 1991). However, C. mydas, E. imbricata, and foraging define the Tagbanua people’s identity and removing this 71 7 olive ridley (Lepidochelys olivacea) nesting sites are widespread component of their lives would endanger their culture (Dalabajan 72 8 Q7 throughout the Philippines (Cruz 2002; Ramirez-de Veyra 1994). 2001). The Tagbanua people hunt marine turtles and collect their 73 9 Other sites with published data available include: Mindanao (Byrne eggs according to traditional management practices such as cul- 74 10 and Hines 2005; Quimpo 2013); Northeastern Palawan (Ladra and tural taboos and sacred areas (Guieb 2010; Sampang 2007). Addi- 75 11 Laguidao 1992); Panay and Guimaras Islands (Bagarinao 2011); tionally, the Philippines’ National Protected Area System strongly 76 12 Panikian Island, and Morong (Cruz 2002). Encouragingly, the promotes the inclusion of indigenous peoples and the integration 77 13 Pawikan (marine turtle) Conservation Project, established in June of their traditional ecological knowledge in natural resource man- 78 14 1979, has achieved much towards the sustainable management of agement strategies (Capistrano 2010). 79 15 turtles in the Philippines, including the development and imple- Here we report on a rapid assessment of marine turtle pop- 80 16 mentation of conservation and protection policies, management ulations in the Calamian Islands that combines social and ecological 81 17 and propagation schemes, and nationwide information and edu- approaches, to provide information urgently required for conser- 82 18 Q8 cation programs (Ramirez-de Veyra 1994; Sagun 2003; Trono vation efforts including distribution of key nesting sites and pat- 83 19 1991). terns of exploitation. 84 20 The Calamian Islands (Figure 1) support a rich diversity of ma- 85 21 rine habitats including coral reefs, beaches, and seagrass beds Materials and methods 86 22 (Garces et al 2013; Tupper et al 2015), providing important foraging 87 23 and nesting grounds for marine turtles. At least four of the world’s In order to rapidly develop a deeper understanding of marine 88 24 seven species of marine turtles have been historically reported in turtle distribution, we carried out interviews in a total of 15 bar- 89 25 the islands’ coastal waters (PCSDS 2006a,b,c,d): nesting pop- angays located throughout the Calamianes (a barangay is the 90 26 ulations of C. mydas and E. imbricata, occasional transient logger- smallest administrative division in the Philippines; a village, dis- 91 27 heads (Caretta caretta; Sagun 2003) and leatherbacks (Dermochelys trict, or ward). Interview-based approaches have been employed in 92 28 coriacea; Salinas et al 2009). Human exploitation for meat and eggs, several studies of marine species globally (Moore et al 2010), 93 29 combined with degradation of nesting and foraging sites and providing a low-cost, rapid means of acquiring information over 94 30 incidental capture in local fisheries, are major threats (PCSDS large areas. Barangays were selected based on a high occurrence of 95 31 2006a,b,c,d). marine turtle sightings and locally known nesting sites (PCSDS 96 32 97 33 98 34 99 35 100 36 101 37 102 38 103 39 104 40 105 41 106 42 107 43 108 44 109 45 110 46 111 47 112 48 113 49 114 50 115 51 116 52 117 53 118 54 119 55 120 56 121 57 122 58 123 59 124 60 125 61 126 62 127 63 128 64 Figure 1. Location of the Calamian Islands showing marine turtle nesting sites identified during the current study, sites labeled in red indicate presence of body pits during surveys 129 65 (for site names, see Tables 1 and A1). 130

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1 2006a,b,c,d) and logistical considerations (sites that were remote Results 66 2 and difficult to access were not surveyed). Barangay captains, heads 67 3 of fishing associations, and octopus fishers (who fish in shallow All KIs were aware of the presence of marine turtles in the 68 4 coastal habitats, strongly associated with marine turtles) assisted Calamianes; species mentioned in descending frequency were 69 5 us in the identification of individuals particularly knowledgeable C. mydas (31 respondents, n ¼ 36, 86.1%), E. imbricate (27 re- 70 6 about turtles and their nesting sites [hereafter referred to as key spondents, n ¼ 36, 75.0%), D. coriacea (4 respondents, n ¼ 36, 11.1%), 71 7 informants (KIs)]. We utilized a qualitative questionnaire consisting and C. caretta (2 respondents, n ¼ 36, 5.6%). C. mydas and 72 8 entirely of open answers to maximize the richness and detail of E. imbricata were confirmed by KIs as nesting in the area. D. coriacea 73 9 information gained (Newing 2011). We aimed to elucidate infor- and C. caretta were only reported to be observed at sea. Nesting 74 10 mation on marine turtle nesting sites and behavior, patterns of sites identified by qualitative interviews and focus group discus- 75 11 exploitation, and local knowledge of conservation status and legal sions are given in Tables 1 and A1. A total of 37 beaches were sur- 76 12 protection. veyed in situ and a total of 47 turtle body pits were recorded at 16 77 13 Interviewees were generally approached in their place of work, beaches (Table 1). Pamalican Island, LinamodioeBuenavista and 78 14 and questioned on an individual basis in local dialects. Questions GaloceTototan were identified as the beaches with the highest 79 15 covered the following: marine turtle nesting site distribution, nesting densities of > 10 body pits/km (Table 1). 80 16 hunting, cultural practices, and understanding of conservation Qualitative interviews suggested that marine turtles nest all 81 17 status. We used photographs to confirm species identification with year round in the Calamianes, since there was no consensus 82 18 KIs, especially noting key anatomical differences between species. established among KIs on peak nesting seasons (January, 7 re- 83 19 Interviews were undertaken until it was considered that little spondents, 19.4%; February, 5 respondents, 13.9%; March, 5 re- 84 20 important new information or understanding relevant to the spondents, 13.9%; April, 6 respondents, 16.7%; May, 14 respondents, 85 21 research questions was being elucidated, i.e., according to the 38.9%; June, 7 respondents, 19.4%; July, 6 respondents, 16.7%; 86 22 principle of saturation (Newing 2011). August, 7 respondents, 19.4%; September, 4 respondents, 11.1%; 87 23 A total of 36 interviews were conducted from November 2014 to October, 5 respondents, 13.9%; November, 10 respondents, 27.8%; 88 24 February 2015: 16 in Busuanga, 11 in Coron, and nine in Culion. and December, 7 respondents, 19.4%; n ¼ 36). Most respondents (26 89 25 Access to a number of sites was impossible because of the North respondents, n ¼ 36, 72.2%) had observed hatchlings emerging 90 26 East Monsoon (amihan). Focus group discussions were therefore from nests and swimming in the open ocean among Sargassum 91 27 also used to gather information from the remotest areas. These algae. Respondents recalled observing predominantly C. mydas 92 28 discussions were held at a workshop using the qualitative ques- hatchlings (15 respondents, n ¼ 26, 57.7%), but also E. imbricata (10 93 29 tionnaire to structure the dialogue. KIs were a mixture of fishers, respondents, n ¼ 26, 38.5%). In general, KIs had an accurate un- 94 30 local environmental officials, caretakers and managers of privately derstanding of marine turtle reproductive and foraging ecology, 95 31 owned islands, and a turtle hunter. Ages ranged from 24 years to 69 although, notably, most (32 respondents, n ¼ 36, 88.9%) did not 96 32 years, with a mean age of 36 years. know the age at which turtles reach sexual maturity. 97 33 We also conducted rapid assessments of nesting activity from KIs all noted that opportunistic hunting was a major threat to 98 34 November 2014 to January 2015 using standardized IUCN marine turtles in the Calamianes and it was clear that hunting and 99 35 methods (Schroeder and Murphy 1999) on the principal nesting egg collection continued to be actively practiced in the area, 100 36 beaches identified by the aforementioned qualitative interviews focusing on nesting sites (Tables 1 and A1). Hunters were noted to 101 37 and previous studies (PCSDS 2006a,b,c,d; Figure 1, Tables 1 and be primarily Tagbanua (12 respondents, n ¼ 36, 33.3%), but also 102 38 A1). We aimed to determine the relative importance of beaches residents of Tara (1 respondent, n ¼ 36, 2.8%) and Maglalambay (1 103 39 for marine turtle nesting and associated patterns of exploitation, respondent, n ¼ 36, 2.8%) Islands, and migrants from the Visayas (3 104 40 with body pit densities providing an indicator of the relative respondents, n ¼ 36, 8.3%), Mindoro (3 respondents, n ¼ 36, 8.3%), 105 41 importance of sites. Body pits are excavations made by a female Cuyo Islands (1 respondent, n ¼ 36, 2.8%), and the Batangas (1 106 42 turtle on the beach just prior to digging the egg chamber respondent, n ¼ 36, 2.8%). Turtles were not only hunted for sub- 107 43 Q9 (Hendrickson 1958). Global Positioning System (GPS) coordinates sistence as a reliable, cheap source of protein (25 respondents, 108 44 were taken at the start and end of each surveyed area of beach at 109 45 the high tide line, with beach length calculated by recording 110 46 tracks with the GPS. Nesting activity was measured in terms of the 111 Table 1. Details of beaches in the Calamian Islands where evidence of turtle nesting 47 total number and density of body pits per km of beach surveyed. was observed in situ during surveys. 112 48 The GPS location of each body pit, distance from the high tide line 113 Site (municipality) * No. of Body pit Known for Turtle 49 and general habitat was recorded. Body pits were marked to avoid 114 body pits density/km hunting remains 50 repeat recording. Species-level identification was limited by: (1) 115 UU 51 the absence of tracks to aid in identification (tracks being more 1 Pamalican Island (B) 6 19.47 116 2 LinamodioeBuenavista (Co) 3 16.30 52 ephemeral in nature compared to body pits (Mortimer and Day 3 GaloceTototan (Cu) 3 10.49 U 117 53 1999) and thus more susceptible to loss to the elements); and 4 GaloceDikabinton (Cu) 3 8.00 U 118 54 (2) the erosion of body pits, which hindered identification based 5 Maltatayoc (B) 3 7.67 119 55 on size and depth. 6 Club Paradise (Co) 3 7.01 120 7 Panlaitan Island (B) 8 6.84 U 56 Turtle remains provided evidence of exploitation at the beaches 121 8 Turda Kalibunan (Co) 5 5.92 57 surveyed. Remains were assumed to be the result of human 9 North Cay (B) 2 5.56 122 58 exploitation: (1) due to their presence on beaches making it un- 10 South Cay (B) 1 4.85 123 59 likely the turtle died at sea; and (2) from any marks visible on the 11 GaloceLabinton (Cu) 3 3.97 U 124 e U 60 remains. Remains were identified to species level when possible 12 Galoc Sabang (Cu) 1 3.47 125 13 Papachilin (B) 1 2.88 61 and their location recorded. Obvious signs of damage (e.g., contact 14 DecapedianeDecabobo (Co) 3 2.31 126 62 of flippers with propellers, hooks, or other man made instruments, 15 Diwaran Island West (Co) 1 1.60 U 127 63 or penetration of the carapace) indicated cause of death. Where the 16 Diwaran Island East (Co) 1 0.98 U 128 64 turtle appeared to have been killed for food, notes were made on B ¼ Busuanga; Co ¼ Coron; Cu ¼ Culion. 129 65 what meat had been taken and what had been left behind. * Site number corresponds to the map in Figure 1. 130

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1 n ¼ 36, 69.4%), but were also sold for income (7 respondents, n ¼ 36, sustainable. Balancing indigenous rights with conservation goals 66 2 19.4%); one KI mentioned that Chinese residents in Coron were will be particularly challenging. It is important that local commu- 67 3 regular buyers. Cultural traditions of the Tagbanua were also dis- nities understand turtle life history, in particular slow maturation 68 4 cussed, with turtle meat typically served as the main dish at rates and ramifications for susceptibility to overexploitation. 69 5 weddings, birthdays, and funerals. Furthermore, addressing overseas demand for turtle products must 70 6 The primary turtle hunting tools were spears (18 respondents, be a focus of wildlife law enforcement agencies. Clearly, areas that 71 7 n ¼ 36, 50.0%), fishing nets (11 respondents, n ¼ 36, 30.6%), and combine evidence of high levels of nesting activity and exploitation 72 8 hooks (7 respondents, n ¼ 36, 19.4%). Spears with a line attached should be prioritized for protection. The sites which were found to 73 9 were used in the open ocean and hunters believed that a few drops host significant nesting sites, but which were also noted as hunting 74 10 of their saliva on the spearhead would ensure that the turtle could grounds included: Galoc Island, Pamalican Island, and Panlaitan 75 11 not escape. Nets and hooks were also commonly used at sea, with Island. Approaches to marine turtle research and conservation that 76 12 hooks employed to pierce the neck and flippers. Mataya Reef on the capitalize on traditional knowledge may also provide an opportu- 77 13 east coast of Coron was mentioned as an important hunting ground nity to involve the Tagbanua in marine conservation initiatives. The 78 14 (Figure 1; Table A1). On nesting beaches, turtles were caught by traditional ecological knowledge of the Tagbanua could provide 79 15 hand with the hunter straddling the turtle’s back and immediately intergenerational evidence of changes in marine turtle occurrence 80 16 tying up the flippers with rope. One KI also noted that turtles were in the Calamianes and this information could complement scien- 81 17 sometimes accidentally trapped in fish corrals. Prices for turtle tific data to provide more effective and inclusive management of 82 18 meat ranged from US$ 4.50 for a live subadult; US$ 0.70/kg meat up turtle populations (Berkes et al 2000). 83 19 to US$ 33.50e67.00/kg for boiled and dried scutes. 84 20 During the beach surveys, three C. mydas remains were Acknowledgments 85 21 encountered: (1) a carapace at Pamalican beach, suspected to have 86 22 been used for cooking due to burn marks on the carapace and re- We are grateful to the Department of Natural Resources, Pala- Q10 87 23 mains of cooking fires in the area; (2) a head on the beach at wan Provincial Government for funding this work, the C3 88 24 Mabinchilao Island and (3) a plastron hanging from a tree in Bak- Philippines field team for their hard work and the numerous local 89 25 tatan, Galoc Island. The meat had already been taken, and the people who so gladly provided the benefit of their expertise and 90 26 plastron was destined to be made into a local guitar. In addition, it knowledge of marine turtles. Credit is also due to two anonymous 91 27 was also mentioned that E. imbricata were not hunted, as eating reviewers who provided useful comments on an earlier draft of this 92 28 their meat “causes all your previous sicknesses to come back” and manuscript. 93 29 the eggs are unpalatable because of their strong flavor of fish. 94 30 The majority (28 respondents, n ¼ 36, 77.8%) of KIs were aware Appendix A 95 31 of local and national laws that protect marine turtles and prohibit 96 32 hunting. It was widely noted that marine turtle populations were in 97 33 need of protection to ensure their sustainability and stated that 98 34 local residents and fisher folk should be the stakeholders primarily Table A1. List of marine turtle nesting sites identified by key informants in the 99 Calamian Islands. 35 responsible for their conservation. 100 36 Site Municipality Nesting Known for Turtle 101 37 Discussion assessment hunting Remains 102 38 conducted 103 39 Our data show that marine turtles are widely distributed 17 Mabichilao Busuanga U U 104 UU 40 18 Black Island Busuanga 105 throughout the Calamianes, albeit at relatively low densities, U fi 19 Cheey Busuanga 41 including con rmed nesting populations of C. mydas and 20 CheeyeSitio Minuit Busuanga U 106 42 E. imbricata (Figure 1). The extensive seagrass beds around the 21 New Quezon Busuanga U 107 43 islands are likely to be important foraging grounds for C. mydas and 22 Old Busuanga Busuanga U 108 44 the coral reefs critical habitat for E. imbricata (Garces et al 2013; 23 San Isidro 1 Busuanga U 109 24 San Isidro 2 Busuanga U 45 Tupper et al 2015). Thus, the Calamian Islands may be considered 110 25 San Rafael Busuanga U 46 a critical site for marine turtles because they provide a full com- 26 LajalaeCYC Coron U 111 47 plement of habitats to support multiple life history stages. Isolated, 27 LajalaeDimanlit Coron U 112 48 small islands, in particular Pamlaican and the islands south of 28 Marcilla Coron U 113 e U 49 Busuanga and off the northwest of Culion, appear to host important 29 Napascud Buenavista Coron 114 30 Turda Batacalan Coron U 50 nesting beaches (Figure 1). No clear peak nesting season was 31 Turda Floro Coron U 115 51 determined in this study, although a previous study in the vicinity 32 Turda Kalampisaw Coron U 116 52 noted a peak during the North East Monsoon between October and 33 Turda Matoyoctoyoc Coron U 117 53 March (Ladra and Laguidao 1992). 34 Pass Island Culion U 118 35 GaloceDaladan Culion UU 54 The Tagabanua were identified as the most prolific turtle 119 36 GaloceBaktatan Culion UUU 55 hunters in the Calamianes and are legally permitted to take turtles 37 Bgy. Buluang Busuanga U 120 56 according to their ancestral rights and cultural traditions (Guieb 38 Calauit Island Busuanga U 121 57 2010). The growing black market for turtle products, including 39 Debotunay Island Busuanga U 122 U 58 the presence of overseas buyers, is of particular concern, as it be- 40 East Nalaut Island Busuanga 123 U fi 41 Malatnubung Island Busuanga 59 comes increasingly dif cult to distinguish between legal indige- 42 Midpid Island Busuanga U 124 60 nous harvest and illegal commercial exploitation (Humber et al 43 Sitio Lakdayan Busuanga U 125 61 2014). Restricted logistical access to isolated islands which host 44 West Nalaut Island Busuanga U 126 62 nesting sites also hinders effective law enforcement. 45 Cabilauan Island Coron U 127 46 Mataya Reef Coron U 63 Engagement with the indigenous communities of the region, to 128 47 GaloceSimparan Culion U 64 whom these species are traditionally and culturally valuable, will 48 GaloceTimpas Culion U 129 65 be a first step in ensuring that any permitted turtle harvest is 49 Lamud Island Culion U 130

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