Marine Turtle Newsletter Issue Number 156 January 2019

Three rescued juvenile green turtles from the Gulf of Venezuela (see pages 41-43). Photo credit: GTTM-GV, Laboratory of General Ecology-University of Zulia, Venezuela.

Articles Nesting Green Turtle Tagged in Cuba, Recaptured in Florida...... F Moncada et al. First Record of Green Turtle Nesting in Almofala, Western Coast of Ceará, Brazil...... EHSM Lima et al. The Threat of Predatory Fire Ants to Loggerhead Turtles Nesting on Jekyll Island, Georgia, USA...... CT Holbrook et al. Sea Turtle Observations On and Around Siniya Island, Umm Al Quwain, United Arab Emirates...... R Whelan et al. Turtle Watching - Combining Conservation and Tourism: A Case Study in New Caledonia...... TC Read et al. Identification ofChelonia mydas Populations in Saudi Arabia Through Regional Genetic Analyses...... MP Jensen et al. Unusual Mortality Event of Leatherback Turtles in the Southern Coast of São Paulo State, Brazil...... SM Nagaoka et al. Rescue and Rehabilitation of Loggerhead Sea Turtles from Dahanu Coast, Maharashtra, India...... P Hatkar et al. A Juvenile Loggerhead Turtle Tagged in Cuba Is Recaptured in Colombian Waters...... F Moncada et al. Using Bamboo Nest Covers to Prevent Predation on Sea Turtle Eggs...... E Korein et al. Albinism In Florida Green Turtle (Chelonia mydas) Hatchlings: Ratio-Based Evidence Of Basic Mendelian Recessiveness...... JR Perrault & CM Coppenrath Marine Debris and Marine Turtles in the Venezuelan Guajira Peninsula: A New Menace...... H Barrios-Garrido et al.

Reports Recent Publications

Marine Turtle Newsletter No. 156, 2019 - Page 1 ISSN 0839-7708 Editors: Managing Editor: Kelly R. Stewart Matthew H. Godfrey Michael S. Coyne The Ocean Foundation NC Sea Turtle Project SEATURTLE.ORG c/o Marine Mammal and Turtle Division NC Wildlife Resources Commission 1 Southampton Place Southwest Fisheries Science Center, NOAA-NMFS 1507 Ann St. Durham, NC 27705, USA 8901 La Jolla Shores Dr. Beaufort, NC 28516 USA E-mail: [email protected] La Jolla, California 92037 USA E-mail: [email protected] Fax: +1 919 684-8741 E-mail: [email protected] Fax: +1 858-546-7003

On-line Assistant: ALan F. Rees University of Exeter in Cornwall, UK

Editorial Board:

Brendan J. Godley & Annette C. Broderick (Editors Emeriti) Nicolas J. Pilcher University of Exeter in Cornwall, UK Marine Research Foundation, Malaysia

George H. Balazs ALan F. Rees National Marine Fisheries Service, Hawaii, USA University of Exeter in Cornwall, UK

Alan B. Bolten Kartik Shanker University of Florida, USA Indian Institute of Science, Bangalore, India

Robert P. van Dam Manjula Tiwari Chelonia, Inc. Puerto Rico, USA National Marine Fisheries Service, La Jolla, USA

Angela Formia Oğuz Türkozan University of Florence, Italy Adnan Menderes University, Turkey

Colin Limpus Jeanette Wyneken Queensland Turtle Research Project, Australia Florida Atlantic University, USA

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Marine© Turtle Marine Newsletter Turtle No. Newsletter 156, 2019 - Page 1 Nesting Green Turtle Tagged in Cuba, Recaptured in Florida

Félix Moncada1, Christina M. Coppenrath2,3, Sarah Hirsch2, Gonzalo Nodarse4, Annie Page-Karjian5, Ashley M. Reeves6 & Justin R. Perrault2 1Centro de Investigaciones Pesqueras. 248 No. 0603, e/5ª ave y mar, Santa Fe, Playa, La Habana, Cuba (E-mail: fmoncada@ cip.alinet.cu); 2Loggerhead Marinelife Center, 14200 U.S. Highway One, Juno Beach, Florida 33408 USA (E-mail: jperrault@ marinelife.org, [email protected]); 3Florida Atlantic University, 777 Glades Road, Boca Raton, Florida 33431 USA (christina. [email protected]); 4Marina Marlin Cayo Largo, Isla de la Juventud, Cuba (E-mail: [email protected]); 5Harbor Branch Oceanographic Institute, Florida Atlantic University, 5600 U.S. Highway One, Fort Pierce, Florida 34946 USA; 6University of Tennessee College of Veterinary Medicine, 2407 River Drive, Knoxville, Tennessee 37996 USA (E-mail: [email protected])

A nesting green turtle (Chelonia mydas) originally tagged in July tag remained secure in the turtle’s right front flipper. In addition 2009 in Cayo Largo, Cuba, was observed nesting in Juno Beach, to measurements and tagging, blood, skin samples, and cloacal Florida (Fig. 1) eight years later in July 2017. This is an interesting swabs were collected for health and virology assessments. This case of a green turtle nesting at two distant and very different sites: turtle appeared to be in good health based on gross observation and Cayo Largo (Cuba: insular, southern coast, extends east-west) plasma biochemistry and hematology results. She tested negative and Juno Beach, Florida (USA: peninsular/continental, east coast, for chelonid herpesvirus 5 (ChHV5) based on quantitative PCR extends north-south). analysis of whole blood targeting the UL30 gene segment of the The turtle was originally tagged in the right front flipper with a ChHV5 genome (after Page-Karjian et al. 2015), and enzyme-linked titanium tag (CB1728) by Marina Marlin staff during a nighttime immunosorbent assays [ELISA] targeting plasma antibodies to nesting survey as a part of a project aimed at marking nesting ChHV5 and lung-eye-trachea virus (LETV, after Coberley et al. females on the beaches in this important tourist area. This project 2001 and Herbst et al. 2008). was a part of the Fisheries Research Center (CIP-Cuba) “Tagging The observation of this turtle nesting in Cayo Largo and later Program,” which has been tagging sea turtles on nesting beaches, on Juno Beach, Florida is a rare and interesting case pertaining to in hatcheries, and in foraging habitats throughout the Cuban the natal philopatry of green sea turtles. Philopatry is a distinctive archipelago since 1989. CB1728 was tagged on 21 July 2009 while characteristic of marine turtles, where individuals return to nest on nesting on Mal Tiempo beach in Cayo Largo (Fig. 2). Cayo Largo, beaches in the same geographic areas where they hatched (Bowen located at the eastern end of the Canarreos archipelago (located off et al. 1992). This behavior is then translated into genetic differences southwestern Cuba), is one of the busiest nesting sites for green between nesting populations that are sufficiently geographically and loggerhead (Caretta caretta) turtles in the Cuban archipelago, and an important nesting site for green turtles in the Wider Caribbean region (Medina et al. 2009, Nodarse et al. 2010). The turtle measured 106.5 cm curved carapace length (CCL) when first tagged. In the same year (2009), the turtle was observed nesting two additional times on Mal Tiempo beach (30 July and 10 August). On 7 July 2013, she was observed nesting on Lindamar Beach, three km east of Mal Tiempo Beach, where she was initially tagged (Fig. 2). CB1728 was next observed nesting ~600 km away in Juno Beach, Florida on 7 July 2017 (Fig. 1), during nightly surveys conducted by Loggerhead Marinelife Center (LMC) staff. The turtle measured 107.1 cm CCL, indicating little growth (<0.1 cm/yr) since her initial encounter in 2009. A passive integrated transponder (PIT) tag (#989001001238897; frequency: 134.2 kHz; Biomark®, Inc., Boise, Idaho) was implanted into her right front flipper in addition to a new Inconel tag being added to the trailing edge of her left front flipper (EEN106). The CB1728

Figure 1. Geographic location of Cayo Largo, Cuba and Juno Beach, Florida USA. Marine Turtle Newsletter No. 156, 2019 - Page 1 Figure 2. Location of Cayo Largo and spatial location of its beaches. distant (Bowen & Karl 2007). This observation supports MEDINA, Y., F. MONCADA, G. NODARSE & R. BLANCO. mitochondrial haplotype frequencies in the Wider Caribbean, 2009. Anidación de la tortuga verde (Chelonia mydas) y suggesting stock contribution and connectivity between green turtles caracterización de las playas en Cayo Largo, Cuba. Revista in the region (Moncada et al. 2006; Shamblin et al. 2012). Cubana de Investigaciones Pesqueras 26: 66-72. It is important to note that many of the nesting green turtles tagged MONCADA, F., F.A. ABREU-GROBOIS, A. MUHLIA-MELO, in Cayo Largo appear to forage primarily in the coastal waters of C. BELL, S. TRÖENG, K.A. BJORNDAL, A.B. BOLTEN, Nicaragua (Moncada et al. 2016) and satellite telemetry data have A.B. MEYLAN, J. ZURITA, G. ESPINOSA, G. NODARSE, revealed that Cuban green turtles are highly migratory throughout R. MÁRQUEZ-MILLÁN, A. FOLEY & L. EHRHART. 2006. the Wider Caribbean (Ruiz 2017). This is the first observation Movement patterns of green turtles (Chelonia mydas) in Cuba of a green turtle from Cayo Largo nesting on another nesting and adjacent waters inferred from flipper tag recaptures. Journal beach outside of the archipelago. This recapture provides support of Herpetology 41: 22-34. for genetic studies, which generally indicate some population MONCADA, F.G., C.J. LAGUEUX, G. NODARSE, Y. MEDINA, connectivity between these two nesting populations and suggests R. BLANCO & J. AZANZA. 2016. Marine turtle migrations from that these turtles might transit between the north and south coasts the Cuban shelf to coastal waters of Nicaragua. In: Belskis, L., A. of the Cuban shelf, or beyond (Moncada et al. 2006). Frey, M. Jensen, R. LeRoux & K. Stewart (Comps.). Proceedings Acknowledgements. We thank the workers of Marina Marlin (Cayo of the 34th Annual Symposium on Sea Turtle Biology and Largo, Cuba), who have been tagging sea turtles for decades in Cayo Conservation. NOAA Tech Memo NMFS-SEFSC-701. pp. 169. Largo through the “Tagging Program.” NODARSE, G., F.G. MONCADA, Y. MEDINA, C. RODRÍGUEZ, BOWEN, B.W., A.B. MEYLAN, J.P. ROSS, C.J. LIMPUS, G.H. F. HERNÁNDEZ, R. BLANCO & E. ESCOBAR. 2010. BALAZS & J.C. AVISE. 1992. Global population structure and Comportamiento de la anidación de tortugas marinas en los Cayos natural history of the green turtle (Chelonia mydas) in terms of San Felipe y Archipiélago de los Canarreos, Cuba (2001-2006). matriarchal phylogeny. Evolution 46: 865-881. Revista Cubana de Investigaciones Pesqueras 27: 66-71. BOWEN, B.W. & S.A. KARL. 2007. Population genetics and PAGE-KARJIAN, A., T.M. NORTON, B. RITCHIE, C.C. BROWN, phylogeograpy of sea turtles. Molecular Ecology 16: 4886-4907. C. MANCIA, M. JACKWOOD & N.L. GOTTDENKER. COBERLEY, S.S., L.H. HERBST, D.R. BROWN, L.M. EHRHART, 2015. Quantifying chelonid herpesvirus 5 in symptomatic and D.A. BAGLEY, S.A. SCHAF, R.H. MORETTI, E.R. JACOBSON asymptomatic rehabilitating green turtles (Chelonia mydas). & P.A. KLEIN. 2001. Detection of antibodies to a disease- Endangered Species Research 28: 135-146. associated herpesvirus of the green turtle, Chelonia mydas. Journal RUIZ, C. 2017. Identificación de posibles áreas de alimentación of Clinical Microbiology 39: 3572-3577. de Chelonia mydas (Testudines, Cheloniidae) del archipiélago HERBST, L.H., S. LEMAIRE, A.R. ENE, D.J. HESLIN, L.M. cubano. BSc Thesis, Havana University, Havana, Cuba. 58pp. EHRHART, D.A. BAGLEY, P.A. KLEIN & J. LENZ. 2008. Use SHAMBLIN, B.M., K.A. BJORNDAL, A.B. BOLTEN, Z.M. of baculovirus-expressed glycoprotein H in an enzyme-linked HILLIS-STARR, I. LUNDGREN, E. NARO-MACIEL & C.J. immunosorbent assay developed to assess exposure to chelonid NAIRN. 2012. Mitogenomic sequences better resolve stock fibropapillomatosis-associated herpesvirus and its relationship to structure of southern Greater Caribbean green turtle rookeries. the prevalence of fibropapillomatosis in sea turtles. Clinical and Molecular Ecology 21: 2330-2340. Vaccine Immunology 15: 843-851.

Marine Turtle Newsletter No. 156, 2019 - Page 2 First Record of Green Turtle (Chelonia mydas) Nesting in Almofala, Western Coast of Ceará, Brazil

Eduardo H. S. M. Lima, Maria Thereza D. Melo & Fernando Diógenes Alves Ferreira Fundação Pró-TAMAR, Acesso Projeto TAMAR, 131 Almofala, CEP: 62592-000, Ceará, Brazil (E-mail: [email protected])

Green turtles (Chelonia mydas) are globally distributed throughout participation into the conservation efforts have brought great tropical and subtropical waters along continental coasts and oceanic success to the protection of sea turtles in Brazil (Silva et al. 2016). islands. Early juveniles spend most of their lives in pelagic waters, Flipper tagging data have indicated a connection between Ceará thereafter, they move to shallow coastal areas, usually associated and the Caribbean, regarding this species. Genetic analyses based with submerged banks of sea grass and algae. In the Atlantic Ocean, on mitochondrial DNA indicated that juvenile green turtles found major green turtle rookeries are found in Florida, Ascension Island, at Almofala originate mainly from Ascension Island, but also from Tortuguero (Costa Rica), Aves island (Venezuela), Suriname, and Matapica (Suriname), Aves Island (Venezuela) and Tortuguero Brazil, among others (Penaloza, 2000; Broderick et al. 2006; (Costa Rica), and possibly from other nesting areas in the Atlantic, Chaloupka et al. 2008; Almeida et al. 2011; Naro-Maciel et al. such as Trindade Island (Lima et al. 2013). 2014). The main nesting sites along the Brazilian coast are in The results presented here place the conservation of sea turtles the oceanic islands of Trindade (Espírito Santo), Atol das Rocas off the Ceará coast in an international context. Although the exact (Rio Grande do Norte) and Fernando de Noronha (Pernambuco). reason for sporadic nesting remains unknown, protecting areas However, occasional nesting has been documented in the mainland of occasional sea turtle occurrence is extremely important for the coasts of Bahia, Rio Grande do Norte, Sergipe and Espírito Santo conservation of these animals in the future. States (Almeida et al. 2011). Acknowledgements. The authors thank Raimundo Lelé, for The state of Ceará is an important feeding ground for five species kindly informing us about the green turtle nest and Dr Daphne of sea turtles (Chelonia mydas, Caretta caretta, Dermochelys W. Goldberg for the helpful comments and careful reading of the coriacea, Lepidochelys olivacea and Eretmochelys imbricata). manuscript. Projeto TAMAR is officially sponsored by Petrobras. However, C. mydas is the most common species. The area hosts a Pró-TAMAR Foundation is the main executor of the National Action mixed stock of green turtles originating from Suriname, Ascension Plan for the Conservation of Sea Turtles in Brazil (NAP), from Island, Trinidad and Tobago, Nicaragua and French Guiana (Lima ICMBio (Chico Mendes Institute for Biodiversity Conservation)/ et al. 2003; Naro-Maciel et al. 2006; Marcovaldi et al. 2010; Lima MMA. Data collection was authorized by ICMBio, through special et al. 2013). license number 14122-12, issued by Biodiversity Authorization and Almofala Beach is a small fishing community located on the Information (SISBIO). west coast of Ceará State, with approximately 11,500 inhabitants, ALMEIDA, A.P., A.J.B.S. SANTOS, J.C.A. THOMÉ, C. BELINI, most of them having descended from Tremembé Indians, whose C. BAPTISTOTTE, M.Â. MARCOVALDI, A.S. SANTOS & M. livelihoods involve fishing and agriculture. According to fishermen, LOPEZ. 2011. Avaliação do Estado de Conservação da Tartaruga about 50 years ago, sea turtle nesting used to occur on a regular basis. Marinha Chelonia mydas (Linnaeus, 1758) no Brasil. Biodiversidade However, a long history of exploitation and direct consumption of Brasileira 1: 12-19. sea turtles eggs and meat have depleted whole populations. On 8 March 2017 a green turtle nest was found on Almofala ALMEIDA, A.P., L.M.P. MOREIRA, S.C. BRUNO, J.C.A. Beach, 2.9117 °S, 39.8466 °W, located near the city of Itarema, in THOMÉ, A.S. MARTINS, A.B. BOLTEN & K.A. BJORDAL. Ceará, Northeastern Brazil. The nest was left in situ and monitored 2011. Green turtle nesting on Trindade Island: abundance, trends, closely until it hatched on 4 May - 57 days after it was laid. The and biometrics. Endangered Species Research. 14: 193-201. nest was then excavated to confirm the species identification, to BRODERICK, A.C., R. FRAUENSTEIN, F. GLEN, G.C. HAYS, calculate hatching success and to release hatchlings that could not A. JACKSON, T. PELEMBE, G.D. RUXTON & B.J. GODLEY. exit the egg chamber by themselves. 2006. Are green turtles globally endangered? Global Ecology and The clutch size was 130 eggs, of which 64 produced live Biogeography 15: 21-26. hatchlings, 63 were undeveloped eggs (with no detectable sign of CHALOUPKA M., K.A. BJORNDAL, G.H. BALAZS, A.B. embryonic development) and three were unhatched dead embryos. BOLTEN, L.M. EHRHART, C.J. LIMPUS, H. SUGANUMA, The hatching success of the eggs was estimated to be 49.2%. The S. TROËNG & M. YAMAGUCHI. 2008. Encouraging outlook hatchlings were released in a public ceremony with the Mayor of for recovery of a once severely exploited marine megaherbivore. Itarema and other government members. The event was part of a Global Ecology and Biogeography 17: 297-304. strategy for creating awareness about sea turtle conservation in the LIMA, E.H.S.M., C.J. LAGUEUX, P.C.R. BARATA & M.Â. region. MARCOVALDI. 2003. Second record of a green turtle (Chelonia In 1993, Projeto Tamar established a research station in Almofala mydas) tagged in Brazil and captured in Nicaragua. Marine Turtle aiming to reduce incidental capture in fisheries. The protection Newsletter 101: 27-28. strategies as well as its initiatives to bring fisher and local community Marine Turtle Newsletter No. 156, 2019 - Page 3 LIMA, E.H.S.M., M.T.D. MELO, M.H. GODFREY & P.C.R. NARO-MACIEL, E., J.H. BECKER, E.H.S.M. LIMA, M.Â. BARATA. 2013. Sea turtles in the waters of Almofala, Ceará, MARCOVALDI & R. DESALLE. 2006. Testing dispersal in Northeastern Brazil, 2001–2010. Marine Turtle Newsletter hypotheses in foraging green sea turtles (Chelonia mydas) of 137: 5-9. Brazil. Journal of Heredity 98: 29-39. MARCOVALDI, M.Â., G.G. LOPEZ, L.S. SOARES, E.H.S.M. PENALOZA, C. 2000. Demografia y viabilidad de la poblacion LIMA, J.C.A. THOMÉ & A.P. ALMEIDA. 2010. Satellite de tortuga verde, Chelonia mydas, en Isla de Aves. BSc Thesis, tracking of female loggerhead turtles highlights fidelity behavior Universidad Simon Bolivar, Sartenejas, Venezuela. 87pp. in northeastern Brazil. Endangered Species Research 12: 263-272. SILVA, V.R.F., S.F. MITRAUD, M.L. CAMARGO, E.H.S.M. NARO-MACIEL E., B.N. REID, S.E. ALTER, G. AMATO, K.A. LIMA, M.T.D. MELO, A.J.B. SANTOS, A.C.C.D. SILVA, J.C. BJORNDAL, A.B. BOLTEN, M. MARTIN, C.J. NAIRN, B. CASTILHOS, J.A.F. BATISTA, G.G. LOPEZ, F. TOGNIN, J.C. SHAMBLIN & O. PINEDA-CATALAN. 2014. From refugia to THOMÉ, C. BAPTISTOTTE, B. GALLO, J.H. BECKER, J. rookeries: phylogeography of Atlantic green turtles. Journal of WANDERLINDE, F. PEGAS, G. ROSTAN, G.G. MARCOVALDI Experimental Marine Biology and Ecology 461: 306-316. & M.Â. MARCOVALDI. 2016. Adaptive threat management framework: Integrating people and turtles. Environment Development and Sustainability 18: 1541-1558.

Marine Turtle Newsletter No. 156, 2019 - Page 4 The Threat of Predatory Fire Ants to Loggerhead Turtles Nesting on Jekyll Island, Georgia, USA

C. Tate Holbrook1, John W. Mahas1,2, Breanna L. Ondich3 & Kimberly M. Andrews3,4 1Department of Natural Sciences, College of Coastal Georgia, Brunswick, GA, USA (E-mail: [email protected]); 2Department of Entomology and Plant Pathology, Auburn University, Auburn, AL, USA (E-mail: [email protected]); 3Jekyll Island Authority Georgia Sea Turtle Center, Jekyll Island, GA, USA (E-mail: [email protected]); 4Odum School of Ecology, University of Georgia, Athens, GA, USA (E-mail: [email protected])

Sea turtles worldwide face a barrage of threats including fisheries al. 2003). Few attempts have been made to measure the frequency bycatch, directed take, pollution, pathogens, climate change, and of nest infestation by fire ants, but estimates range from 8.3% of coastal development that degrades and destroys nesting habitat loggerhead nests in Wassaw National Wildlife Refuge (WNWR), (National Research Council 1990; Mast et al. 2005). Moreover, GA from 1992-1994 (Moulis 1997), to 21.6% in Cape San Blas, FL efforts to manage beaches for sea turtle nesting can be undermined from 1997-1998 (Parris et al. 2002), to as many as half of all nests by predation of eggs and hatchlings by native and introduced species. at Main Beach in Key West National Wildlife Refuge, FL in 1994 Therefore, minimizing nest depredation has been identified as a key (Wilmers et al. 1996). Moreover, Moulis (1997) found evidence objective of recovery plans for the loggerhead turtle (Caretta caretta) of reduced emergence success in loggerhead nests containing ants. and other species (NMFS-USFWS 2008). In the Northwest Atlantic Given the widespread distribution of fire ants on nesting beaches loggerhead population, common nest predators include armadillos of the loggerhead, green turtle (Chelonia mydas), and other species (Dasypus novemcinctus), coyotes (Canis latrans), feral hogs (Sus of concern, it is important to investigate the extent and impacts of scrofa), fire ants Solenopsis( spp.), foxes (Urocyon cinereoargenteus predation, thereby elucidating the need for targeted management and Vulpes vulpes), ghost crabs (Ocypode quadrata), and raccoons and intervention (NMFS-USFWS 2008). (Procyon lotor) (Dodd 1988; Drennen et al. 1989; NMFS-USFWS Our objective was to assess the threat of predatory ants to 2008). The impacts of mammalian predators, in particular, are loggerhead turtles nesting on Jekyll Island (JI), GA, USA. Using well-documented and can be quite severe, prompting longstanding a decade of nest monitoring data (2007-2016), we estimated the predator control and nest protection programs (Engeman et al. frequency of nest depredation by fire ants, explored habitat and nest 2006; NMFS-USFWS 2008). In contrast, the threat of loggerhead factors that might influence the vulnerability of sea turtle nests to nest depredation by ants has received less attention (but see sources ant infestation, and quantified impacts on loggerhead reproductive reviewed below), and more research on its prevalence, potential risk success. Ants collected from predation events during the 2015-2016 factors, and associated losses is needed to devise and implement nesting seasons were identified to species. appropriate management plans. Jekyll Island is a 2,238-ha barrier island state park managed by Several predatory ant species, including the native tropical fire the Jekyll Island State Park Authority (JIA). The island has over ant, Solenopsis geminata, and a thief ant, Solenopsis globularia, 15 km of dynamic beaches, which are transformed annually by are known to attack sea turtle eggs or hatchlings in the southeastern erosion and accretion. Each km-long section of beach is permanently United States (LeBuff 1990; Moulis 1997). However, the most marked at its southern end (Fig. 1). While some stretches of beach notorious is the red imported fire ant, Solenopsis invicta, an are undeveloped, others are backed by residential and commercial invasive species that was introduced from South America via the development. Historical management practices including the port of Mobile, Alabama in the 1930s and expanded throughout flattening of dunes and the construction of approximately 5 km the Southeast by the 1970s (Callcott & Collins 1996). Solenopsis of rock revetment have diminished the suitable sea turtle nesting invicta is an effective predator of numerous vertebrate species, the habitat (Ondich & Andrews 2013). most vulnerable being oviparous, ground-nesting birds and reptiles The loggerhead is the predominant sea turtle species nesting including turtles (reviewed by Allen et al. 2004). on JI, with green turtle and leatherback (Dermochelys coriacea) Depredation of loggerhead nests by S. invicta has been reported nests occurring more rarely. Initiated in 1972, the Jekyll Island from locales in Georgia (GA; Moulis 1997) and Florida (FL; Sea Turtle Project has continuously monitored the loggerhead Wilmers et al. 1996; Parris et al. 2002), and surveys indicate that nesting population through various phases of management, funding, S. invicta occurs on many, if not most, sea turtle nesting beaches in methodology, and effort (Ondich & Andrews 2013). Nest monitoring both states, often in great abundance (Allen et al. 2001; Wetterer has been coordinated by the JIA Georgia Sea Turtle Center (GSTC) et al. 2007; Braman, C.A., pers. comm.). Fire ants have been since its establishment in 2007. observed penetrating and feeding on sea turtle eggs prior to pipping The dataset analyzed here includes 1,394 loggerhead nests (Moulis 1997; Diffie et al. 2010) and attacking, injuring, killing, laid between 2007 and 2016. During those years, daily night and and consuming hatchlings from the time the hatchlings pip through morning patrols were conducted throughout the nesting season their emergence onto the beach surface (Wilmers et al. 1996; (night patrols from mid-May through July; morning patrols from Moulis 1997; Parris et al. 2002). Moreover, loggerhead hatchlings May until hatchlings emerged from the final nest, usually in early stung by S. invicta can suffer increased mortality up to 12 days October). Nests were either monitored in situ or relocated a short later, either directly due to envenomization or indirectly through distance away when they were deposited in vulnerable areas at risk secondary infection, disorientation, or decreased vigor (Krahe et of erosion or tidal inundation. Predation by raccoons and foxes was Marine Turtle Newsletter No. 156, 2019 - Page 5 Low detectability has excluded non-mammalian predators from previous assessments of sea turtle nesting success (Lindborg et al. 2016). We consider our estimates of losses to predation by ants to be conservative. To test whether ant infestation was associated with loggerhead nest features or reproductive success, we conducted χ2 tests of independence for nominal variables and Mann-Whitney U tests for continuous variables, most of which were non-normally distributed. We elected not to perform a logistic regression analysis for several reasons, including: (1) multiple regression would exclude cases missing any data (e.g., 5 years of “distance from vegetation”) and further reduce the sample size for ant-depredated nests; (2) we did not aim to construct a model to predict the likelihood of nest depredation; and (3) the tests we employed make fewer assumptions and are more straightforward to interpret than logistic regression models. Statistical analyses were conducted using SPSS 24 (IBM Corp.). During 2015-2016, samples of ants were collected from 18 Figure 1. Location of Jekyll Island, Georgia, USA. The depredated loggerhead nests. Specimens were preserved in 95% numbers represent markers placed at the southern end of ethanol and later identified to species by CTH and JWM using keys most sections; km 0 continues from the northern tip of the by Trager (1991) and MacGown (2014). Species identifications were island to the southwest, and km 15 extends northward from confirmed by C.A. Braman (University of Georgia) and voucher the km 14 marker. The southern tip of the island has accreted specimens were deposited in the College of Coastal Georgia insect since the map was generated; the km 13 marker is positioned collection. at the current location. Across 10 nesting seasons from 2007 to 2016, predation by ants managed using protective screening placed over nests; most recently, was directly observed in 79 of 1,210 loggerhead nests (6.5%). The the project used 1.2×1.2 m pieces of screening made of 97% recycled frequency of nest depredation ranged from 3.3% of nests in 2011 high-density polyethylene with a 5×5 cm mesh (MasterNet LTD to 14.4% of nests in 2014, with no consistent pattern of increase product number MN-L77). or decrease over time (Table 1). Ant activity without evidence of Nests were typically excavated on the fifth day following the predation was documented in another 45 nests, including 20 of the 46 first sign of hatchling emergence, or 70 days after deposition if nests that were excavated early upon the discovery of intruding ants, no signs of hatchling emergence were observed. Forty-six nests for a total of 124 (10.2%) nests with ants present. If all loggerhead were excavated early when ants were observed entering the egg nests are included (i.e., those lost to erosion or unknown causes, chamber. During excavation, technicians recorded the numbers of and other failed nests with unhatched eggs), and we assume that hatched eggs (eggshell fragments > 50% intact), unhatched eggs, ants feeding on eggs in failed nests were scavengers, then only live hatchlings, and dead hatchlings inside the nest, as well as the presence of ants (loosely identified as “fire ants”) and any evidence Total Nests (%) of predation. Clutch size was estimated as the sum of hatched and Year nestsa depredated by ants unhatched eggs. After the nest was excavated, nest depth was measured from the beach surface to the bottom of the egg chamber. 2007 43 3 (7.0%) From 2012-2016, we also measured the distance between the nest 2008 124 7 (5.6%) and the primary line of dune vegetation, with negative numbers 2009 64 3 (4.7%) denoting nests located seaward of the vegetation line and positive numbers denoting nests located landward of the vegetation line. 2010 130 5 (3.8%) We compiled and reviewed all records of predation and other 2011 151 5 (3.3%) activity by ants. A predation event was scored only when ants 2012 178 8 (4.5%) were directly observed entering viable eggs or feeding on live or 2013 143 13 (9.1%) newly deceased hatchlings in the nest or during emergence. The analysis excluded nests that were completely lost to erosion (n = 2014 90 13 (14.4%) 56 “wash-outs”) or unknown causes (n = 13) because it is unlikely 2015 135 14 (10.4%) that predation occurring prior to those losses would have been 2016 152 8 (5.3%) detected. We also excluded nests that failed to hatch for reasons other than predation (arrested development; microbial, fungal, or Total 1210 79 (6.5%) plant root invasion; n = 115) because scavengers of decaying eggs Table 1. Number (percentage) of loggerhead nests could not reliably be distinguished from predators. It is possible depredated by ants on Jekyll Island, GA, USA from 2007- that some incidences of ants scavenging on dead hatchlings were 2016. aExcludes nests lost to erosion or unknown causes and misclassified as predation, but it is also likely that our methods other failed nests with unhatched eggs, where predation by failed to detect additional predation events, especially egg predation. ants could not reliably be detected. Marine Turtle Newsletter No. 156, 2019 - Page 6 sting and are not known to prey on vertebrates. Therefore, S. invicta Nests (%) is the most likely candidate for incidences of loggerhead nest Total depredated depredation attributed to “fire ants” between 2007-2014, when ants Km nests by ants General habitat zone(s)a were not collected or identified to species. More extensive surveys 0 2 0 dynamic inshore flat beach are underway to describe the diversity and distribution of ants on 1 82 3 (3.7%) dynamic beach backed by pine JI and throughout the GA coast, and to better understand the threat forest; tree boneyard they pose to sea turtles and beach-nesting shorebirds. 2 21 1 (4.8%) tree boneyard Predation events were unevenly distributed across the 15+ km of beaches on JI (Table 2). The small samples of nests in some beach 3 3 0 rock revetment armoring sections and the coarse scale of the habitat data limit our ability 4 0 0 rock revetment armoring to infer associations between nesting habitat and predation risk. 5 1 0 rock revetment armoring Nonetheless, it is noteworthy that the majority of ant-depredated nests (51 of 79 or 65%) were located between km 6 and 10 along the 6 51 5 (9.8%) rock revetment armoring most heavily developed beachfront with some of the busiest public 7 40 8 (20.0%) rock revetment armoring access points. It remains to be tested whether human disturbance and 8 148 17 (11.5%) dunes backed by development food sources promote higher densities of fire ants on recreational beaches, as proposed by Wilmers et al. (1996). 9 110 9 (8.2%) dunes backed by development Fire ants and other beach-dwelling ants typically nest in 10 189 12 (6.3%) dunes backed by development partially shaded, vegetated areas of dunes, rather than on open 11 197 7 (3.6%) natural tall dunes beach, although they may venture onto the latter to forage. It has 12 154 5 (3.2%) natural tall dunes; accretional therefore been suggested that sea turtles nesting in closer proximity flat beach to dune vegetation are more vulnerable to attack by ants (LeBuff 1990; Wetterer et al. 2007). On a beach in Palm Beach County, FL, 13 121 6 (5.0%) accretional flat beach; Wetterer et al. (2007) found that more ants were attracted to baits erosional inshore dunes on sea turtle nests that were closer to dune vegetation. Moreover, 14 80 6 (7.5%) erosional inshore dunes; tree Moulis (1997) reported that loggerhead nests infested by fire ants boneyard in WNWR, GA were generally located within a meter of the dune 15 11 0 dynamic inshore flat beach vegetation line, indicating a possible “edge effect.” In contrast, we found that loggerhead nests located at least 1 m seaward of the Table 2. Distribution of ant-depredated loggerhead nests primary vegetation line were just as likely to be depredated by ants by section (km) of beach, with corresponding habitat characterization. aDetermined by GSTC in 2017 (Bishop & (21 of 232 nests) as nests within 1 m of the vegetation line in either direction (12 of 219 nests) or at least 1 m landward of the vegetation Marsh 1999; Jackson et al. 2012; Georgia Coastal Hazards 2 Portal http://gchp.skio.uga.edu). line (22 of 244 nests; χ = 2.624, df = 2, P = 0.269). However, our test of the distance-to-vegetation hypothesis was limited by the relatively 5.7% of nests were depredated by ants, though that is probably an narrow width of suitable nesting habitat between the dunes and high underestimate given the low likelihood of detecting predation in tide line on JI beaches; the most distant ant-depredated nest was 7.4 those additional nests. m below the vegetation line, well within the estimated foraging range Of 42 ant-depredated nests with sufficiently detailed records, of S. invicta colonies (Martin et al. 1998; Tschinkel 2011), with only evidence of egg consumption was documented in six nests, including 15 non-depredated nests located farther away. For comparison, on the presence of ant-sized entrance holes, whereas attacks on the wider beach surveyed by Wetterer et al. (2007), the percentage hatchlings were more commonly observed in 37 nests. Ants were of nests (baits) with ants present declined most sharply beyond 10 found covering live and dead hatchlings inside the egg chamber m seaward of the vegetation line. and as they emerged from the nest. The bodies of some hatchlings Nest relocation away from high-risk areas is a controversial were swollen, particularly around the eyes, and others appeared management practice with complex, context-dependent costs and to be disoriented on the beach, possibly resulting from fire ant benefits (McElroyet al. 2015). One potential negative consequence stings (Krahe et al. 2003). When recorded, the number of attacked of relocating nests is increased exposure to nest predators including hatchlings ranged from 1 to 71 per nest, although in some cases fire ants, which may be attracted to the human-disturbed sites. additional hatchlings may have been spared from predation when However, rates of predation by ants did not differ between in situ technicians intervened. nests (65 of 1015 or 6.4% were depredated) and relocated nests All ants collected from depredated nests in 2015-2016 were (14 of 195 or 7.2% were depredated; χ2 = 0.161, df = 1, P = 0.688). identified as S. invicta. Two other Solenopsis species that are Moreover, the lack of a distance-to-vegetation effect (above) reported to attack sea turtles - the tropical fire ant,S. geminata, and suggests that relocating nests at risk of tidal inundation or wash-out a thief ant, S. globularia (LeBuff 1990; Moulis 1997; Wetterer et al. to higher ground does not necessarily make them more vulnerable 2016) - have been documented on other barrier islands in GA but to predatory ants. not on JI (Ipser et al. 2004; C.A. Braman, pers. comm.). Preliminary Next, we examined two internal nest factors that might influence surveys indicate that pyramid ants (Dorymyrmex spp.) are abundant the likelihood of depredation by ants: nest depth and clutch size. along sea turtle nesting beaches on JI and could potentially be We hypothesized that shallower nests and larger clutches may be confused with fire ants by a lay observer; however, they cannot more easily detected by fire ants, which use olfactory cues to search Marine Turtle Newsletter No. 156, 2019 - Page 7 It was previously reported that loggerhead nests depredated by S. invicta produced fewer emergent hatchlings, though success rates were estimated from a relatively small sample without inferential statistics (Moulis 1997). In our study, ant-depredated nests suffered only a slight, non-significant reduction in emergence

success (mediannon-depredated = 79.0%, mediandepredated = 69.9%; U =

26537, n1 = 53, n2 = 1107, P = 0.24). It is possible that a stronger effect of predation on emergence success may have been obscured by numerous other sources of variation that were not controlled (Lindborg et al. 2016). We did discover a higher proportion of dead

hatchlings in ant-depredated nests (U = 59784, n1 = 78, n2 = 1108, P < 0.001), also noted by Moulis (1997). Moreover, emergence success fails to account for predation after hatchlings exit the nest; although emergence events were rarely observed in real time, we encountered as many as 22 hatchlings being attacked by fire ants on the surface of one nest, and S. invicta stings have been shown to cause delayed post-emergence mortality (Krahe et al. 2003). Figure 2. Clutch size of loggerhead nests that were In conclusion, predatory ants pose yet another threat to the nesting depredated by ants (n = 78) versus those that were not success of sea turtles. On JI and throughout much of the southeastern depredated by ants (n = 1,121). Boxes represent 1st and 3rd USA, the primary concern is the red imported fire ant, S. invicta, quartiles with medians. Whiskers are min and max within which has recently spread to important sea turtle nesting beaches in 1.5 times the interquartile range excluding outliers (◦). the West Indies as well (Davis et al. 2001; Wetterer & Snelling 2006). for food via a network of underground foraging tunnels that extend The risk of nest depredation by fire ants likely varies geographically from their own nests and open to the surface (Tschinkel 2006). and may depend on habitat and nest features such as clutch size, Although nest depth did not differ between ant-depredated and though in the absence of experimentation, the mechanisms of fire non-ant-depredated in situ nests (U = 12952, n1 = 46, n2 = 508, P ant–sea turtle interactions remain largely unknown. Predation by = 0.222), clutch size did vary in the predicted direction: nests that ants is one of many factors that may influence sea turtle reproductive were depredated by ants contained larger clutches (median = 112.5 success, with potential consequences for population recovery eggs) than nests that were not depredated by ants (median = 106 (NMFS-USFWS 2008). However, population-level effects could eggs; U = 50887, n1 = 78, n2 = 1121, P = 0.015; Fig. 2). be negligible if a small proportion of nests is infested, with only a Further research is needed to explain the positive association minor reduction in average emergence success, as indicated on JI; between clutch size and nest infestation by ants. Fire ant foragers more data and population modeling are required to determine the may be attracted to the greater area and/or duration of disturbance degree of impact. Nevertheless, we appeal to sea turtle managers created when loggerhead females dig larger nests and lay more to be vigilant, assess the local threat of ants on managed beaches, eggs, or to specific cues emanating from large clutches, such as and consider targeted control methods when warranted, feasible, the amplified scent of mucous, decaying eggs or eggshells, and/ and environmentally responsible. or hatchlings in the nest. Alternatively, if there is greater variance Acknowledgments. We extend our sincere appreciation to T. Norton, in hatching/emergence time within larger clutches, then faster- K. Mascovich, J. Colbert, and GSTC for their instrumental support; developing hatchlings may draw attention to their slower-developing all the staff, volunteers, interns, and AmeriCorps members who nestmates. The delayed emergence of sea turtle hatchlings from the have sustained the Jekyll Island Sea Turtle Project for many years; nest could make them more susceptible to predation by ants; newly C. Braman for confirming ant identifications and reviewing the hatched loggerheads typically remain in the egg chamber for at manuscript; and S. Coleman and J. Miller-Martin for insightful least two days before emerging (Miller et al. 2003). Fire ants have discussion. Funding was provided by a College of Coastal Georgia been shown to establish underground foraging tunnels into the nests Summer Research Fellowship to C.T.H. of freshwater turtles with delayed emergence (Allen et al. 2001; ALLEN, C.R., D.M. EPPERSON & A.S. GARMESTANI. 2004. Buhlmann & Coffman 2001). Red imported fire ant impacts on wildlife: a decade of research. Finally, we tested for effects of predation by ants on loggerhead American Midland Naturalist 152: 88-103. reproductive success, as measured by hatching success (the number of hatchlings leaving their eggs) and emergence success (the number ALLEN, C.R., E.A. FORYS, K.G. RICE & D.P. WOJCIK. 2001. of hatchlings reaching the beach surface, Miller et al. 2003; McElroy Effects of fire ants (Hymenoptera: Formicidae) on hatching turtles et al. 2015). The 46 nests that were excavated prior to 5-days post and prevalence of fire ants on sea turtle nesting beaches in Florida. emergence were excluded from the analysis because they may have Florida Entomologist 84: 250-253. contained viable eggs/hatchlings yet to hatch/emerge, while losses BISHOP, G.A. & N.B. MARSH. 1999. Sea turtle nesting habitat to predation may have been minimized when ant invasions were assessment: a rapid, integrated, technological approach. In: interrupted. Hatching success did not differ between ant-depredated Proceedings of the University System of Georgia Rock Eagle and non-ant-depredated nests (U = 29444.5, n1 = 53, n2 = 1107, P = Annual Technology Conference. pp. 1-15. 0.964), which was not surprising given the relatively low frequency BUHLMANN, K.A. & G. COFFMAN. 2001. Fire ant predation of of egg predation we observed. turtle nests and implications for the strategy of delayed emergence. Marine Turtle Newsletter No. 156, 2019 - Page 8 Journal of the Elisha Mitchell Scientific Society 117: 94-100. McELROY, M.L., M.G. DODD & S.B. CASTLEBERRY. 2015. CALLCOTT, A.A. & H.L. COLLINS. 1996. Invasion and range Effects of common loggerhead sea turtle nest management expansion of imported fire ants (Hymenoptera: Formicidae) in methods on hatching and emergence success at Sapelo Island, North America from 1918-1995. Florida Entomologist 79: 240- Georgia, USA. Chelonian Conservation & Biology 14: 49-55. 251. MILLER, J.D., C.J. LIMPUS & M.H. GODFREY. 2003. Nest DAVIS, L.R., JR., R.K. VANDER MEER & S.D. PORTER. 2001. site selection, oviposition, eggs, development, hatching, and Red imported fire ants expand their range across the West Indies. emergence of loggerhead turtles. In: Bolten, A.B. & B.E. Florida Entomologist 84: 735-736. Witherington (Eds.). Loggerhead Sea Turtles. Smithsonian Institution Press, Washington, D.C. pp. 125-143. DIFFIE, S., J. MILLER & K. MURRAY. 2010. Laboratory observations of red imported fire ant (Hymenoptera: Formicidae) MOULIS, R.A. 1997. Predation by the imported fire ant Solenopsis( predation on reptilian and avian eggs. Journal of Herpetology invicta) on loggerhead sea turtle (Caretta caretta) nests on Wassaw 44: 294-296. National Wildlife Refuge, Georgia. Chelonian Conservation & Biology 2: 433-436. DODD, C.K., JR. 1988. Synopsis of the biological data on the loggerhead sea turtle Caretta caretta (Linnaeus 1758). US Fish NMFS (NATIONAL MARINE FISHERIES SERVICE) & USFWS and Wildlife Service, Biological Report 88(14). 110pp. (US FISH AND WILDLIFE SERVICE). 2008. Recovery plan for the Northwest Atlantic population of the loggerhead sea turtle DRENNEN, D., D. COOLEY & J.E. DEVORE. 1989. Armadillo (Caretta caretta), 2nd revision. NMFS. Silver Spring, MD. 325pp. predation on loggerhead turtle eggs at two national wildlife refuges in Florida, USA. Marine Turtle Newsletter 45: 7-8. NATIONAL RESEARCH COUNCIL. 1990. Decline of the Sea Turtles: Causes and Prevention. National Academies Press, ENGEMAN, R.M., R.E. MARTIN, H.T. SMITH, J. WOOLARD, Washington, D.C. 280pp. C.K. CRADY, B. CONSTANTIN, M. STAHL & N.P. GRONINGER. 2006. Impact on predation of sea turtle nests ONDICH, B.L. & K.M. ANDREWS. 2013. A history of sea turtle when predator control was removed midway through the nesting tagging and monitoring on Jekyll Island, Georgia, USA. Marine season. Wildlife Research 33: 187-192. Turtle Newsletter 138: 11-15. IPSER, R.M., M.A. BRINKMAN, W.A. GARDNER & H.B. PARRIS, L.B., M.M. LAMONT & R.R. CARTHY. 2002. Increased PEELER. 2004. A survey of ground-dwelling ants (Hymenoptera: incidence of red imported fire ant (Hymenoptera: Formicidae) Formicidae) in Georgia. Florida Entomologist 87: 253-260. presence in loggerhead sea turtle (Testudines: Cheloniidae) nests and observations of hatchling mortality. Florida Entomologist JACKSON, C.W., C.R. ALEXANDER & D.M. BUSH. 2012. 85: 514-517. Application of the AMBUR R package for spatio-temporal analysis of shoreline change: Jekyll Island, Georgia, USA. TRAGER, J.C. 1991. A revision of the fire ants,Solenopsis geminata Computers & Geosciences 41: 199-207. group (Hymenoptera: Formicidae: Myrmicinae). Journal of the New York Entomological Society 99: 141-198. KRAHE, H., J.K. WETTERER & L.D. WOOD. 2003. Impact of fire ant stings on sea turtle hatchling survival. In: Seminoff, J.A. TSCHINKEL, W.R. 2006. The Fire Ants. The Belknap Press of (Comps.). Proceedings of the 22nd Annual Symposium on Sea Harvard University Press, Cambridge, MA. 723pp. Turtle Biology and Conservation. NOAA Tech Memo NMFS- TSCHINKEL, W.R. 2011. The organization of foraging in the fire SEFSC-503. pp. 211-212. ant, Solenopsis invicta. Journal of Insect Science 11: 26. LEBUFF, C.R., JR. 1990. The Loggerhead Turtle in the Eastern WETTERER, J.K., M.J. LILES, J.M. SERMEÑO, L.S. Gulf of Mexico. Caretta Research Inc., Sanibel, Florida. 236pp. CERVANTES, E.E. ECHEVERRIA, R.M.E. HERNÁNDEZ, LINDBORG, R., E. NEIDHARDT, B. WITHERINGTON, J.R. A. HENRIQUEZ, D. PÉREZ, D.A.S. GARCÍA, C.E.G. SMITH & A. SAVAGE. 2016. Factors influencing loggerhead PERALTA, R.L. SORTO & G. MELENDEZ. 2016. Predaceous (Caretta caretta) and green turtle (Chelonia mydas) reproductive fire ants (Hymenoptera: Formicidae) at sea turtle (Testudines: success on a mixed use beach in Florida. 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HUTCHINSON, E. HOWGATE & N.J. Imported fire ants Solenopsis( invicta): a growing menace to sea PILCHER. 2005. MTSG update: IUCN/SSC Marine Turtle turtle nests in Key West NWR. In: Keinath, J.A., D.F. Barnard, J.A. Specialist Group hosts the second Burning Issues Assessment Musick & B.A. Bell (Comps.). Proceedings of the 15th Annual Workshop. Marine Turtle Newsletter 110: 13-15. Symposium on Sea Turtle Biology & Conservation. NOAA Tech Memo NMFS-SEFSC-387. pp. 341-343. Marine Turtle Newsletter No. 156, 2019 - Page 9 Sea Turtle Observations On and Around Siniya Island, Umm Al Quwain, United Arab Emirates

Roxanne Whelan, Chris Clarke, Rob Gubiani & Sabir Bin Muzaffar Department of Biology, College of Science, United Arab Emirates University, PO Box 15551, Al Ain, UAE (Email: [email protected]; [email protected]; [email protected]; [email protected])

Four species of sea turtles, all listed on the IUCN Red List, occur breeding colony of the regionally endemic Socotra cormorant. It in the Arabian Gulf (Baldwin & Gardner 2005): the Endangered remains one of the largest untouched and natural wetlands areas green (Chelonia mydas, Seminoff 2004), Critically Endangered left in the UAE (Whelan et al. 2017), now threatened by a large- hawksbill (Eretmochelys imbricata, Mortimer & Donnelly 2008), scale development project (https://www.thenational.ae/opinion/ Critically Endangered loggerhead (Caretta caretta, NW Indian sustainable-development-must-not-endanger-birds-1.221624). Ocean subpopulation, Casale 2015) and Vulnerable leatherback We hypothesize that there are critical foraging and nesting (Dermochelys coriacea, Wallace et al. 2013). The Vulnerable olive habitats around Siniya Island. Sea turtles are under threat from ridley (Lepidochelys olivacea, Abreu-Grobois & Plotkin 2008) is various anthropogenic activities within the Gulf. In the UAE, coastal also a visitor to UAE waters (Baldwin & Gardner 2005). Hawksbill development, boat strikes, entanglement in fishing gear and pollution turtles are known to nest in the Arabian Gulf (hereafter named the are all threatening sea turtle populations. No published accounts have Gulf) in large numbers, as do green sea turtles (Pilcher 2000) but been found for hawksbills nesting in the Northern Emirates (or the these nest infrequently in the United Arab Emirates (UAE) (Al southeastern Gulf) including Umm Al Quwain. Recent reports of Suweidi et al. 2012). nesting sea turtles include hawksbill and green turtle nests in Khor Here we report on opportunistic records of both live and stranded Kalba (Sharjah - Arabian Sea coastline, Hebbelmann et al. 2016), sea turtles as well as hawksbill nests found on Siniya Island, (UAE) hawksbill and rare green turtle nests on Sir Bu Nair Island, Sharjah while conducting Socotra cormorant (Phalacrocorax nigrogularis) (within the Gulf, Al Suweidi et al. 2012), a few hawksbill nests field research between 2013 and 2017. Turtle nests were found in on Saadiyat Island, Abu Dhabi (Willing pers. comm.) and other March and April 2015. offshore islands in the Western Region of Abu Dhabi (Baldwin Siniya Island is a small island about 13 km long and is located & Gardner 2005, Al Suweidi et al. 2012) and within the Jebel Ali 2 km off the Umm Al Quwain coastline, one of the least developed Marine Sanctuary, Dubai (Emirates Marine Environmental Group). Emirates in the UAE. The island and its surroundings (Khor Al Beida Through satellite tracking, Siniya Island has been identified as an mangroves) host a variety of habitats including shallow waters, important foraging ground for hawksbill turtles (Pilcher et al. 2014). mudflats, seagrass beds, and mangroves, along with desert scrub Three hawksbill nests and one false crawl were found on the complexes bordering sandy beaches. The shallow subtidal waters northwestern side of the island in 2015 (Table 1, Fig. 1). These around Siniya Island consist of both rocky and sandy substrate with were identified by their asymmetrical flipper tracks which were many sponges - ideal foraging grounds for hawksbills, and important approximately 50 cm wide leading to a body pit and tracks returning habitats for rays and guitarfish (Whelan et al. 2017). It has been to the shore. The tracks were found within a 3-km stretch of a gentle classified by BirdLife International as an ‘Important Bird Area’ with sloping sandbar consisting of fine sand and bordered by vegetation thousands of migrating shorebirds visiting every year, and the largest on a lagoon inlet (Fig. 1). All the eggs had been poached as many

Date Species IUCN Red List Description 18-Nov-14 Eretmochelys imbricata CE Stranding - adult female 4-Jan-15 Eretmochelys imbricata CE Nest, eggs poached 31-Mar-15 Eretmochelys imbricata CE Nest, eggs poached 4-Jul-15 Eretmochelys imbricata CE Nest, eggs poached 4-Jul-15 Eretmochelys imbricata CE False crawl, no nest 23-Oct-16 Eretmochelys imbricata CE Sick small juvenile, rescued 2013-2017 Chelonia mydas E Adults: foraging, travelling 15-Jan-15 Chelonia mydas E Stranding - only carapace 30-Mar-15 Chelonia mydas E Stranding - large adult 5-May-15 Chelonia mydas E Stranding - juvenile 3-Sep-15 Chelonia mydas E Adult, dead in water 26-Jan-16 Chelonia mydas E Stranding - large adult 4-Dec-16 Chelonia mydas E Stranding - large adult Table 1. Opportunistic sea turtle sightings from Siniya Island over a 4-year period (2013-2017). Marine Turtle Newsletter No. 156, 2019 - Page 10 Figure 1. Hawksbill nesting crawls on the northwestern beach of Siniya Island (photos Roxanne Whelan/Chris Clarke). egg shells, digging and human footprints were found around the behavior also reflects this (Pilcher 2014b). Green and hawksbill nests. Most likely these eggs were taken by fishermen working in turtles are important indicators of the health and resilience of Umm Al Quwain and sold at a high price (approximately 50-100 seagrass and reef habitats (Webster 2013). AED = approx. 13-27 USD per egg, Dec 2018 exchange rate) for These sea turtle observations (live and stranded) contribute to consumption (Sultan pers. comm. 2016). sparse data of vulnerable fauna at several life stages in the area Many large adult green turtles have been sighted from the shore around Siniya Island and highlight the need for further monitoring or from the boat foraging on seagrass in shallow waters or in the and beach protection if nests are to successfully hatch, along lagoon inlets (Fig. 2); sightings increased during the months of April with conserving important foraging habitats in Umm Al Quwain. and May (personal observations). One sick juvenile hawksbill turtle Environmental awareness and education for both fishermen and the (approx. 15 cm) was found stranded and covered in barnacles and general public would be key in effective local sea turtle management oysters on 23 October 2016 (Fig. 3). It was rescued and taken to the and conservation. Also, there may be a need to introduce speed Dubai Turtle Rehabilitation Project and later released in May 2017. limits for boats where turtles are known to forage in high numbers. At least seven adult carcasses at various decomposition stages have Acknowledgements. Funding for this work was provided by the been found while surveying the beaches. Some had no obvious cause United Arab Emirates University Program for Advanced Research of death and others had sliced carapaces, likely from boat impacts grant to SBM. Permission to work on Siniya Island was granted (see Fig. 4). The turtles in the Gulf must cope with high salinity by the Municipality of Umm Al Quwain and the Ministry of and seasonal variations in sea temperatures (Sheppard et al. 1992). Hawksbills are generally smaller in size than other hard-shelled sea turtles, which helps them to cope with thermal stress, and their

Figure 2. An adult green turtle in the shallow lagoon (photo: Figure 3. Sick, juvenile hawksbill turtle rescued from Siniya Rob Gubiani). Island (photo: Roxanne Whelan). Marine Turtle Newsletter No. 156, 2019 - Page 11 Figure 4.Photos of stranded turtles included in Table 1. Stranded turtles are regularly found in this stage of decomposition, on the high tide line.

Environment and Water (MOEW). Logistical support was provided BALDWIN, A. CHIKHI, H.S. DAS, S. HAMZA, O.J. KERR, by the Marine Environment Research Center, MOEW. Special A. AL KIYUMI, A. MOBARAKI, H.S. AL SUWAIDI, A.S. AL thanks to Dr. Nicolas Pilcher for confirming the identification based SUWEIDI, M. SAWAF, C. TOURENQ, J. WILLIAMS & A. on turtle tracks. WILLSON. 2014a. Identification of important sea turtle areas ABREU-GROBOIS, A. & P. PLOTKIN. (IUCN SSC Marine Turtle (ITAs) for hawksbill turtles in the Arabian Region. Journal of Specialist Group). 2008. Lepidochelys olivacea. The IUCN Red List Experimental Biology and Ecology 460: 89-99. of Threatened Species 2008: e.T11534A3292503. Downloaded PILCHER, N.J., L. PERRY, M. ANTONOPOULOU, M.A. ABDEL- on 2 May 2017. MOATI, T.Z. AL ABDESSALAAM, M. ALBELDAWI, M. AL AL SUWEIDI, A.S., K.D.P. WILSON, T. HEALY & L. VANNEYRE. ANSI, S.F. AL MOHANNADI, R. BALDWIN, A. CHIKHI, H.S. 2012. First contemporary record of green turtle (Chelonia DAS, S. HAMZA, O.J. KERR, A. AL KIYUMI, A. MOBARAKI, mydas) nesting in the United Arab Emirates. Marine Turtle H.S. AL SUWAIDI, A.S. AL SUWEIDI, M. SAWAF, C. Newsletter 133: 16-17. TOURENQ, J. WILLIAMS & A. WILLSON. 2014b. Short-term behavioral responses to thermal stress by hawksbill turtles in the BALDWIN, R. & D. GARDNER. 2005. Marine reptiles. In: Hellyer, Arabian region. Journal of Experimental Biology and Ecology P. & S. Aspinall. (Eds.). The Emirates: A Natural History. Trident 457: 190-198. Press Limited, London. pp. 243-248. SEMINOFF, J.A. 2004. Chelonia mydas. The IUCN Red List of CASALE, P. 2015. Caretta caretta (North West Indian Ocean Threatened Species 2004: e.T4615A11037468. Downloaded subpopulation). The IUCN Red List of Threatened Species 2015: on 2 May 2017. e.T84127873A84127992. Downloaded on 2 May 2017. SHEPPARD, C., A. PRICE & C. ROBERTS. 1992. Marine ecology HEBBELMANN, L., J. PEREIRA, F. YAGMOUR & A. AL ALI. of the Arabian Region patterns and processes in extreme tropical 2016. New records of sea turtle nesting at Al Qurm Wa Lehhfaiiah environments. Academic Press Limited, London. 359 pp. Protected Area beach after a 30-year absence. Marine Turtle Newsletter 150: 7-9. WALLACE, B.P., M. TIWARI & M. GIRONDOT. 2013. Dermochelys coriacea. The IUCN Red List of Threatened Species 2013: MORTIMER, J.A. & M. DONNELLY. (IUCN SSC Marine Turtle e.T6494A43526147. Downloaded on 2 May 2017. Specialist Group). 2008. Eretmochelys imbricata. The IUCN Red List of Threatened Species 2008: e.T8005A12881238. Downloaded WEBSTER, I. 2013. Observations of green and hawksbill turtles on 2 May 2017. on the southwest coast of Mauritius. Marine Turtle Newsletter 138: 15-17. PILCHER, N.J. 2000. The green turtle, Chelonia mydas, in the Saudi Arabian Gulf. Chelonian Conservation & Biology 3: 730-734. WHELAN, R., R.W. JABADO, C. CLARKE & S.B. MUZAFFAR. 2017. Observations of rays and guitarfish (Batoidea) in shallow PILCHER, N.J., M. ANTONOPOULOU, L. PERRY, M.A. ABDEL- waters around Siniya Island, Umm Al-Qaiwain, United Arab MOATI, T.Z. AL ABDESSALAAM, M. ALBELDAWI, M. Emirates. Tribulus 25: 76-80. AL ANSI, S.F. AL MOHANNADI, N.A. AL ZAHLAWI, R.

Marine Turtle Newsletter No. 156, 2019 - Page 12 Turtle Watching - Combining Conservation and Tourism: A Case Study in New Caledonia

Tyffen C. Read, Marion Petit, Marion Magnan & Richard Farman Laboratory of Marine Biology and Ecology, Aquarium des Lagons, Noumea, New Caledonia (Email: [email protected])

During the 1980s, the interest for sea turtles by tourists greatly collection, invasive species management, and public awareness increased and 59 countries now have some form of sea turtle (Tisdell & Wilson 2002). tourism (Troeng & Drews 2004; Whaling 2017). In his review, Two species, green turtles (Chelonia mydas) and loggerheads Nahill (2011) indicated that 10 million people spend 1.25 billion (Caretta caretta) nest on New Caledonian beaches. The most $USD per year on ecotourism. The favored kind of visit by tourists important nesting site in the region for loggerhead turtles is la Roche is turtle watching during nesting season (Troeng & Drews 2004) but Percée beach, in Bourail (Fig. 1). The nesting turtles of this rookery practices and issues vary according to the countries that feature turtle and Mon Repos rookery (Queensland, Australia) belong to the same watching. A report by the World Wildlife Fund for Nature revealed genetic stock = the east Australian genetic stock (Boyle et al. 2009). that approximately 175,000 people per year visit sites to observe La Roche Percée rookery is the second most important nesting sea turtles with nearly 50% of total tourists divided in three main site for this species in the southwest Pacific (Boyleet al. 2009) with sites worldwide (Troeng & Drews 2004). a yearly nesting population fluctuating from 50 to 80 individuals. Mon Repos Conservation Park was created in 1994, governed In 2006, the Bwärä Tortues Marines Association was created with by the Government of Queensland and Mon Repos Centre is now the main aim of protecting loggerhead turtles at la Roche Percée one of the most famous tourist sea turtle centers in the world, from multiple problems in this touristic site where 120 families live with more than 20,000 visitors per year (Tisdell & Wilson 2005). and where 80% of the nests were being destroyed by local dogs Mon Repos Centre visitors can observe sea turtles while also (Fournière et al. 2015). During the nesting season in 2007/2008, allowing for scientific research on loggerhead turtles by students more than 1,000 visitors came to the beach and tagged along on the and scientists (Tisdell & Wilson 2005). Turtle watching generates daily surveys being conducted but more than 5,000 came during 0.57 million USD$ in direct revenue and 1.7 million USD$ with the 2010/2011 nesting season due to word of mouth. Problems indirect revenue for the region (Tisdell & Wilson 2005), in addition associated with some visitors not following established guidelines to providing various benefits like constant supervision of the nesting (cases of people touching turtles or intoxicated individuals), lack site, revegetation of the landward side of the beach, scientific data of infrastructure, lack of staff and volunteers and the great number

Figure 1.Map of New Caledonia showing the region of Bourail. Marine Turtle Newsletter No. 156, 2019 - Page 13 in New Caledonia. For instance, the visitors were reminded that only Nests laid Hatching authorized personnel were allowed touch the turtle or its eggs, and Nests during tour nests it was strictly forbidden to for tourists to approach a turtle before November 2016 23 12 0 the beginning of the egg-laying activity. Visitors were required to December 2016 102 67 0 remain in the turtle center until they were guided to an identified nesting female turtle on the beach. January 2017 137 61 25 During the wait (1h 45 min average waiting time with a maximum February 2017 41 22 82 of 3h 15 min waiting period), educational aids such as documentaries March 2017 0 0 n/a were shown to visitors, to provide information on the different turtle Total 303 162 107 species, their reproductive cycles, threats, feeding habitats, etc. In addition, documentaries were shown on the New Caledonian lagoon, Table 1. Clutches and hatchling emergences observed and educational movies, games on turtles, and coloring books were during the pilot phase 2016/2017 at La Roche Percée. provided to children. When a turtle was spotted on the beach by the scientific team of of people impacting turtles, daily surveys open to the public were Bwärä Tortues Marines, visitors were invited to reach the nesting stopped in 2012 (Fournière et al. 2015). female following the guide’s instructions. The staff was composed Although a number of countries in the South Pacific islands also of 7 people per night, including Aquarium employees, trainees, have some activities around sea turtles, including Fiji, Solomon summer staff, and volunteers. Each group of visitors on the beach Islands, Micronesia, Vanuatu, etc. (Petro & Fletcher 2007, Tisdell was supervised by two guides at a minimum who positioned the & Wilson 2012, Nichols et al. 2014), there are no guidelines for best visitors >2 m behind the female after the turtle had started laying conservation practices in each country (Whaling 2017). Troeng & eggs. The guides used a small flashlight to show the oviposition Drews (2004) recommended that each site undergo its own studies event. The scientific team recorded the geographical position of to develop specific management plans for sea turtle ecotourism. the nest, checked the female’s identification, tagged the turtle if According to its policy of an economic development respectful of needed with a titanium tag and measured the curved carapace length the environment, the South province of New Caledonia wanted to of the turtle. promote the development of an eco-friendly turtle-watching program A similar setup was organized when hatchling emergence was in in the country. The pilot study was entrusted to the Aquarium des progress on the beach. Visitors followed the guides to the nest and Lagons to define the parameters that would allow the visitors to were arranged in two parallel lines perpendicular to the water. The observe sea turtles during the nesting season but not disturb them. hatchlings were directed towards the sea using a small flashlight The west coastal zone (ZCO) is one of the six sites of the placed low on the sand near the water. “Lagoons of New Caledonia” a UNESCO World Heritage Site During the pilot phase, 2,516 visitors came to observe sea turtles listed in 2008. The entire surface of this zone is 48,200 ha and it is (maximum allowable number was 3,240 visitors). We constrained characterized by proximity to the barrier reef and the coastal area the number of visitors allowed to observe a nesting female to 15. The leading to a “pseudo-lagoon” (Menu & Hébert 2006). The bay of number of observing visitors could be increased but it reduced the Bourail, located in front of a wide opening in the barrier reef, is one quality of the visit, with more people having less direct sight of the of the rare accessible beaches of the west coast with swell (Fig. 1). turtle, and increased challenges to manage a larger group of people. This zone has various remarkable points like la Baie Des Tortues The number of groups able to observe nesting females is directly and la Roche Percée beach, both nesting sites for loggerhead turtles linked to the number of turtles on the beach. In Australia, around but also threatened by various natural and anthropogenic dangers 500 turtles came during the season to lay eggs while there were 50 such as beach erosion, predation by introduced species, and illegal to 80 females seen at La Roche Percée. During the pilot study, 2.5 egg collection. nests were laid per night on average but only 1.2 nests were laid on A pilot study was conducted during the 2016/2017 nesting season average during the opening hours for the visitors. Generally, with with a total of 52 night visits and 20 morning visits to test the 3 groups for 1 turtle per night, it is difficult to satisfy everybody. feasibility and the infrastructure needed for an eco-friendly turtle- The number of turtles being seen by visitors increased in January watching program in New Caledonia. The visitors registered online when hatchling emergence starts and thus visitors have the chance for night visits from 20:00 to 01:00, during December, January to see either a nesting female or emergent hatchlings. and February from Wednesday to Saturday, with a maximum of Throughout the pilot study, 1,070 questionnaires were filled out 45 people per visit, divided in 3 groups of 15 each. Morning visits by visitors. The results showed that only 4.8% of visitors came ran from 05:00 to 07:00 during February, with 45 people maximum from the surrounding region. This can be explained by the fact per morning visit. that local people have already seen egg-laying activities and/or Visitors were invited to park their cars in the first parking lot hatchling emergences, or that residents are not interested in this of La Roche Percée to avoid disturbing nesting turtles with their type of tourist activity. We suspect that local people, who often rely headlights. Visitors were then taken by guides to the turtle center on word of mouth for recommendations, would likely participate (approximately 350 m away). The center was specifically set up more if this activity was to become permanent. Many visitors came for the pilot study with temporary tents away from the beach. from Noumea, the capital of New Caledonia, but tourists from Visitors began the visit with a presentation explaining how the night France represented the majority of visitors. During supervised would progress, the behavior to adopt during the turtle nesting or visits, 88.8% of people saw turtles and 88.2% of them were satisfied emergence, and some reminders of the regulations about sea turtles with the activity. Only 21.5% of visitors thought that the evening Marine Turtle Newsletter No. 156, 2019 - Page 14 group size (15 people) was high against 78% of visitors who were access to the nesting beach by the general public may be helpful. satisfied with group size. For the morning visits, 37.2% of tourists The success of this pilot project suggests that organizing sea said that the group size (45 visitors) was high against 62.8% of turtle tours during the nesting season is viable for New Caledonia people thought the group size was not a problem. Regarding the and less impactful than unsupervised observations. La Roche Percée price, 67% of visitors thought that the ticket price of 1000 F CFP is the most accessible nesting site in New Caledonia and thus (approx. 10 US$) was good value for money, but 40% of tourists suited to support sea turtle ecotourism activity. Further reflection would pay more for the activity. For the morning visits, tourists of sea turtle ecotourism in this area should consider the short- and were brought onto the beach to participate in a “day survey,” where long-term goals. One possible option is to develop a full-scale they participate in conservation activities such as track removal and visitor center and a sea turtle hospital, which could receive visitors hatchling rescue. During the 2 h tour, a maximum 45 visitors walked year-round. This kind of center would also help raise awareness of on the beach (1.7 km long by 40 m wide). During the night visits, turtle conservation within the larger public (families, school groups, the public was on the beach for short periods of time (15-60 min). associations) outside of the nesting season, and create a focal point As an indicator of the negative impact of visitors on nesting female for turtle research in New Caledonia. turtles, we monitored for instances of turtles of returning to the sea Acknowledgements. This pilot study was conducted under permit without laying eggs (false crawl) in the presence of a group during 2966/2016/ARR/DENV. We thank Bwärä Tortues Marines for their the pilot study. There were no false crawls observed in the presence dedication and hard work as well as all the volunteers that helped of groups and the 2016/2017 nesting season was a record year (since during the season, especially Romain Masson, Solène Mora, Norbert 2006) with 86 females. Along with this increase in the number of Douepere and all the others. females (+109% since 2006), there was a record number of nests BOYLE, M.C, N.N. FITZSIMMONS, C.J. LIMPUS, S. KELEZ, laid (328) in 2016/2017 at La Roche Percée rookery. Female turtles X.VELEZ-ZUAZO & M. WAYCOTT. 2009. Evidence for nested 4.4 times on average per season. These data are similar to transoceanic migrations by loggerhead sea turtles in the southern those calculated by the Bwärä Tortues Marines Association (Table Pacific Ocean. Proceedings of the Royal Society B-Biological 1; Fournière et al. 2015). Sciences 276: 1993-1999. When the pilot phase ended, we held meetings with local community members, to gather feedback. Various positive impacts FOURNIÈRE, K., T. JACOB & D. LAFAGE. 2015. Bilan de huit were reported, including: increased turtle nesting activity, improved années de suivi des tortues grosses têtes (Caretta caretta) par beach security (through increased guard presence and reduced l’association Bwärä Tortues Marines et perspectives (sites de la loitering), and large economic benefits for tourist establishments Roche Percée et la Baie des Tortues). Bwärä Tortues Marines: such as campsites, hostels, and inns. Visitors from outside the region Nouméa, New Caledonia. 86pp. of Bourail (95.2% of all visitors) had to stay in different lodging MENU, S. & P. HÉBERT. 2006. Les Lagons de Nouvelle-Caledonie: facilities in the area. Visitors stayed on average 3 days in Bourail and Diversite Recifale et Ecosystemes Associes. Report for World 47% came to the region exclusively to participate to the turtle tours. Hertiage Site Application. Noumea, New Caledonia. 120pp. We also collected data directly from visitors, who reported that NAHILL, B. 2011. Best practices for sea turtle conservation tourism. they stayed 3 days on average in the Bourail region, with 89.9% State of the World’s Sea Turtles Report 7: 18-19. of them staying in touristic housing. Bourail has the capacity NICHOLS, W.J, B. NAHILL & M. GASKILL. 2014. A Worldwide to house 1,160 tourists/night, so the number of visitors was not Travel Guide to Sea Turtles. Texas A&M University Press: College limited by available housing. We estimated 167,000 USD$ in Station, TX, U.S.A. 240pp. economic spinoffs for the region was generated by visitors during the pilot phase. Around 47% of the visitors came exclusively to PETRO, G. & M. FLETCHER. 2007. One small bag for tourists observe sea turtles and an increasing trend was observed during the brings big benefit. SWOT Report 2: 38. season: during December, only 33.2% of visitors came primarily to TISDELL, C.A. & C. WILSON. 2005. Does tourism contribute participate in the pilot phase against 39.7% in January and 63.6% to sea turtle conservation. Is the flagship status of turtles in February. advantageous? Maritime Studies 3-4: 145-167. Turtle watching tours are an important tool for raising public TISDELL, C.A. & C. WILSON. 2012. Nature-based Tourism and awareness and to provide sea turtle knowledge. The guides have Conservation: New Economic Insights and Case Studies. Edward great responsibility in this process, as they have to share quality Elgar Publishing: Cheltenham, U.K. 520pp. information and educational materials to promote awareness about TROENG, S. & C. DREWS. 2004. Money Talks: Economic Aspects sea turtles, their protected species, threats and population dynamics. of Marine Turtle Use and Conservation. WWF-International: Guides also informed the public about rules protecting nesting Gland, Switzerland. 62pp. turtles from possible disturbance, which is especially important as the beach is not closed at night to the general public. WHALING, M. 2017. How Tos for Turtle Tourism: A Review Some things we consider essential to guarantee a positive and of Sea Turtle Tourism, Its Impacts, and Guidelines to Inform respectful turtle guiding project include the following: clear rules Stakeholders in Martinique. MEM Thesis, Duke University, managing actions of visitors must be clearly stated and enforced; Durham, NC. 68pp. guides must be properly trained; in the worst-case scenario, if visitors ignore the rules, then local law enforcement must be willing to help enforce local rules. for the turtle’s safety and satisfied visitors, some rules must be respected. We also suggest that closing nighttime Marine Turtle Newsletter No. 156, 2019 - Page 15 Identification of Chelonia mydas Populations in the Kingdom of Saudi Arabia Through Regional Genetic Analyses

Michael P. Jensen1, Jeff Miller2, Nancy N. FitzSimmons3 & Mustafa Al-Merghani4 1Marine Mammal and Turtle Division, Southwest Fisheries Science Center, NMFS-NOAA, 8901 La Jolla Shores Dr., La Jolla, CA, 92037 USA (E-mail: [email protected]); 2Biological Research and Education Consultants, Missoula, Montana 59801 USA (E-mail: [email protected]); 3Australian Rivers Institute, Griffith University, Nathan, Queensland 4111, Australia (E-mail: [email protected];4 NCWCD (now Saudi Wildlife Authority) P.O Box 61681, Riyadh 11575, Kingdom of Saudi Arabia.

Marine environments of Saudi Arabia provide highly differentiated al. in press) and regional genetic structure of green turtle, Chelonia habitats for nesting and foraging marine turtles in the Red Sea and mydas, populations in the Atlantic (e.g., Lahanas et al. 1994; Arabian (Persian) Gulf. The Red Sea was formed by a long, deep Encalada et al. 1996; Formia et al. 2006 ), south western Indian rift between the continental plates, with limited shallow areas of Ocean (Bourjea et al. 2015), Australasia (e.g., Dethmers et al. 2006; seagrass and reef along the coastal margins (Bruckner et al. 2012; Hamabata et al. 2009), the western Pacific (Dutton et al. 2014b) Bosworth 2015). In contrast, the Arabian (Persian) Gulf is shallow and eastern Pacific (Dutton et al. 2014a). Less is known about the throughout, with large expanses of seagrass and small areas of genetic structure of green turtles in the northwestern Indian Ocean, reef habitat (Sheppard et al. 2010); it is divided into two basins by with the exception of analyses of rookeries at Ras al Hadd in Oman peninsular Qatar. (Reece et al. 2016) and Kuwait (Al-Mohanna et al. 2014), which Widespread, relatively low-density nesting by green turtles analyzed between 352- 487 base pairs of the mtDNA control region (Chelonia mydas) occurs on many beaches throughout the Red from green turtle samples. Sea (Gasperetti et al. 1993) including the Saudi Arabian coastal Here we report on the first study of green turtle population site of Ras Al Baridi (Miller 1989, 2004). A few larger rookeries genetic structure in Saudi Arabia. Blood samples were collected are found along the Egyptian coast and on some offshore islands from nesting green turtles, at Jana Island (n = 11) (27.36877 °N, (El Sadek et al. 2013; Mancini et al. 2015). The majority of green 49.89790 °E) in the Arabian (Persian) Gulf in June 1993 and at Ras turtle nesting is concentrated at Zabargad Island (≈200 females, Al Baridi (n = 16) (24.23066 °N, 37.5227 °E) in the Red Sea in El Sadek et al. 2013) with a smaller concentration (≈50 females) October 1993. DNA was extracted using a salting out procedure as within Wadi Gemal-Hamata National Park (Miller 2004; Hanafy described in Jensen et al. (2013b), and PCR was used to amplify 2012; Mancini et al. 2015). approximately 770 base pairs of the mitochondrial DNA d-loop In the Arabian (Persian) Gulf, the offshore islands of Saudi Arabia using primers LtEi8 and H950g (Abreu-Grobois et al. 2006). host the largest nesting aggregation of green turtles (Miller 1989; Samples were sent to Macrogen, Inc. (Seoul, South Korea) for Pilcher 2000; Miller et al. 2011), with a combined nesting density forward and reverse sequencing. All sequences were aligned and previously estimated to be approximately a thousand turtles per haplotypes determined using Geneious Pro v8.0.2 by doing a blast year (Pilcher 2000). Elsewhere in the Gulf, the distribution of green search against the GenBank database (www.ncbi.nlm.nih.gov/ turtle nesting is uneven and typically low (Gasperetti et al. 1993). blast/). The blast search indicated matches with previously reported Lower density nesting sites occur on islands off Kuwait (Rees et al. shorter sequences, but no match for the longer sequences, so they 2013) and the United Arab Emirates (Miller et al. 2004; Al Suweidi were submitted to GenBank as new haplotypes. et al. 2012). Along the Iranian coast in the Gulf of Oman, hawksbill To determine the genetic population structure in this region, we turtles are the most common nesting species, with some nesting by compared samples from the two Saudi Arabia rookeries to previously green turtles (Mobaraki 2004; Rezaie-Atagholipour & Barmoodeh published green turtle samples from Ras al Hadd in Oman (Reece et 2012). The largest regional green turtle rookery is situated at Ras al. 2016) and Qaruh and Umm Al Maradim in Kuwait (Al-Mohanna al Hadd in Oman (Mendonça et al. 2010). et al. 2014). We used the software Arlequin 3.5 (Excoffier & Lischer

To achieve effective conservation management of marine 2010) to calculate haplotype (h) and nucleotide (π) diversity, FST and species it is necessary to know the spatial extent of populations exact tests for population differentiation between pairs of rookeries. including dispersal and migratory habitat and the interconnection of We tested for genetic isolation by distance using the program habitats used by different life stages. In the case of marine turtles, GeneAlex 6.5 (Peakall & Smouse 2006) to perform a Mantel test on populations typically use one or more rookeries in a region and matrices of distance (natural log of km) and genetic distance (FST/1- their individuals reside across a broad spread of foraging areas, FST). To better understand historic linkages among the rookeries we and conversely, foraging areas are comprised of individuals that constructed a haplotype network for haplotypes found at the four originate from rookeries of different populations. This complexity rookeries using a 95% plausible parsimony network in TCS v1.13 means that an understanding of these dynamics is needed to (Clement et al. 2000) based on previously reported shorter (384) adequately protect the diversity in each species. The definition of mtDNA fragments. management units based on the genetic structure among rookeries We identified four new haplotypes; one haplotype (CmP71.1, supports conservation efforts at a level relevant to the biology of GenBank ID: KP027611) in Ras Al Baridi and three at Jana Island the species (e.g., Jensen et al. 2013a; Matsuzawa et al. 2016). In the (CmP62.1, CmP63.1 and CmP64.1, GenBank ID: KP027608, past decade numerous studies have reported on the global (Jensen et KP027609, KP027610) (Fig. 1 and Table 1). While there was no

Marine Turtle Newsletter No. 156, 2019 - Page 16 Figure 1. Map showing the four Chelonia mydas rookeries located in the Red Sea, Arabian (Persian) Gulf and the northwestern Indian Ocean. Pie charts show the frequency of mtDNA haplotypes found at each rookery. Map created from SEATURTLE.ORG Maptool. 2002. SEATURTLE.ORG, Inc. http://www.seaturtle.org/ maptool/

match for the 770 bp sequences, all four haplotypes matched shorter neighboring Kuwait, less than 300 km away. However, it is important sequences previously identified in Kuwait and Oman (see Table to note the small sample size for the Jana Island Rookery. These 1). Only one haplotype was found in 16 samples from the Ras Al results indicate the existence of at least three unique populations, Baridi rookery in the Red Sea (Table 1). In contrast, three haplotypes or management units, and a putative distinction between the Saudi were present in 11 samples from the Jana Island rookery. This Arabia and Kuwait rookeries in the Arabian (Persian) Gulf that rookery showed high haplotype (h = 0.709) and low nucleotide (π warrants further investigation. The Mantel test revealed a strong = 0.002557) diversity, which was similar to neighboring rookeries isolation by distance effect (r2 = 0.591) where genetic differentiation in Kuwait (Al-Mohanna et al. 2014) (Table 1). The Ras al Hadd between rookeries increased with ocean distance between rookeries. rookery in Oman showed somewhat lower haplotype diversity (h = The haplotype network (384 bp) indicated that three highly 0.688), but much higher nucleotide diversity (π = 0.021664). divergent haplogroups are found in the region (Fig. 2). Haplogroup Significant genetic structure between all pairs of rookeries was A was found only in Ras Al Baridi (Red Sea) and Ras al Hadd found using FST estimates and exact test (Table 2), with the exception (Oman) and it is separated from the other haplotypes by at least 15 of Jana Island and the Qaruh & Umm Al Maradim rookeries in mutational steps. This represents a very old split of genetic lineages

Country Rookery n h SD π SD mtDNA haplotype - 770 base pairs Reference CmP62.1 CmP63.1 CmP64.1 CmP71.1 Saudi Ras 16 0 0 0 0 16 This study Arabia Baridi Saudi Jana 11 0.709 0.083 0.003 0.002 3 5 3 This study Arabia Island mtDNA haplotype 384 base pair CmP62 CmP63 CmP64 CmP71 CmP72 CmP73 CmP49 CmP57 (Cm- (Cm- Reece et al. Oman2) Oman1) 2015 Al- CMKW4 CMKW2 CMKW1 CMKW5 Mohanna et al. 2014 Ras al Reece et al. Oman 42 0.688 0.035 0.022 0.011 15 8 1 17 1 Hadd 2016 Qaruh & Al- Kuwait Umm Al 95 0.673 0.034 0.004 0.003 47 21 13 14 Mohanna et Maradim al. 2014 Table 1. Genetic diversity of samples from Saudi Arabia rookeries and previously published data from Kuwait and Oman rookeries showing sample size (n), haplotype diversity (h), nucleotide diversity (π), standard deviations (SD) and frequency of haplotypes (770 or 384 base pairs). Marine Turtle Newsletter No. 156, 2019 - Page 17 Rookery Rookery Kuwait Jana Is Ras Baridi Oman Qaruh & Umm Al n/a P=0.09570 P <0.00001 P < 0.00001 Maradim, Kuwait Table 2. Tests of genetic 0.053, Jana Island, Saudi Arabia n/a P < 0.00001 P < 0.00001 differentiation between C. mydas P =0.096 rookeries in the Red Sea, Arabian 0.527, 0.698, (Persian) Gulf and northwestern Ras Baridi, Saudi Arabia n/a P < 0.00001 Indian Ocean. Pairwise FST and P =0.000 P =0.000 P values are given below the 0.174, 0.229, 0.473, diagonal and exact test P values Ras al Hadd, Oman n/a P =0.000 P =0.000 P =0.000 are given above the diagonal. that likely dates back millions of years. The three closely related use of samples collected in 1993 warrants that this relationship is haplotypes in Haplogroup B are found in Oman and within the investigated further using newly collected samples and larger sample Arabian (Persian) Gulf. Two haplotypes were found representing sizes. At present, we only find one highly divergent haplotype at Haplogroup C. Both these haplotypes (CmP49 and CmP57) are Ras Al Baridi in the Red Sea, suggestive of a genetic bottleneck. common and widespread through the Indo-Pacific (Bourjea et al. However, additional samples are needed to fully understand the 2007; Jensen et al. 2016). Although the rookery sampled in the population structure within the Red Sea. Red Sea and those in the Arabian Gulf are isolated and share no In contrast, the large green turtle rookery at Ras al Hadd in haplotypes with each other, the rookery in Oman is intermediate, Oman is less isolated and shows evidence of multiple colonization both geographically and genetically. Oman has the only rookery events from at least three divergent lineages resulting in very high to have haplotypes from all three divergent haplogroups and share nucleotide diversity. Most importantly, this study shows that green haplotypes with the Red Sea and the Arabian (Persian) Gulf, as turtles nesting in the region are highly isolated from other regions well as haplotype (CmP49) found at numerous rookeries across the across the Indo-Pacific Ocean and contain two genetic lineages Indo Pacific (Jensenet al. In press). With the exception of CmP49 not found elsewhere in the world. This emphasizes the need for and CmP57, none of the haplotypes found in this region have been effective conservation to protect populations that may contain unique found elsewhere in the world, thus emphasizing the evolutionary evolutionary potential. uniqueness of green turtles in this region. Future research should focus on increasing sample sizes as well These results provide the first genetic study of green sea turtles as characterizing new rookeries to obtain a complete picture of the from the Kingdom of Saudi Arabia and the first comparison of genetic structure in this region. Most of the nesting aggregations population genetic structure of green turtles within the Red Sea, previously mentioned have not been genetically defined and should Arabian (Persian) Gulf and the northwest Indian Ocean. This study be the focus of additional sampling. This will not only provide indicates that there is shallow, but significant, structure among the the basis for accurately defining demographically independent green turtle rookeries within the region. The two rookeries within management units in the region, but will allow researchers to use the Arabian (Persian) Gulf in Kuwait and Saudi Arabia appear genetic tools to identify the rookery origin of turtles from strandings, to belong to the same MU. However, the small sample size and foraging areas and those caught as bycatch in fisheries. Also, the

Figure 2. Haplotype network of eight mtDNA haplotypes (384 bp) found at four rookeries in the Red Sea, Arabian (Persian) Gulf and the northwestern Indian Ocean. Marine Turtle Newsletter No. 156, 2019 - Page 18 use of longer mtDNA sequences has proven to add resolution to Ecology and Evolution 4: 4317-4331. stock structure in some regions (Shamblin et al. 2012; Dutton et DUTTON, P.H., M.P. JENSEN, K. FRUTCHEY, A. FREY, E.L. al. 2014b) and future analyses should use this longer fragment to LACASELLA, G.H. BALAZS, J. CRUCE, A. TAGARINO, R. characterize rookeries. FARMAN & M. TATARATA. 2014b. Genetic stock structure Acknowledgements. We thank the National Commission for of green turtle (Chelonia mydas) nesting populations across the Wildlife, Conservation and Development (now Saudi Wildlife Pacific islands. Pacific Science 64: 451-464. Authority) for administrative and logistical support. ENCALADA, S.E., P.N. LAHANAS, K.A. BJORNDAL, A.B. ABREU-GROBOIS, F.A., J.A. HORROCKS, A. FORMIA, P.H. 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Marine Turtle Newsletter No. 156, 2019 - Page 20 Unusual Mortality Event of Leatherback Turtles (Dermochelys coriacea) in the Southern Coast of São Paulo State, Brazil

Shany Mayumi Nagaoka1, Daniela Ferro de Godoy1,2,3, François Lamou Boussamba4, Angela Formia5 & Guy-Philippe Sounguet4 1Instituto de Pesquisas Cananéia - IPeC, Av. Nina, 532, Retiro das Caravelas, CEP: 11990-000. Cananéia, SP, Brazil (E-mail: [email protected]); 2Programa de Pós-Graduação em Ecologia, Universidade Federal de Juiz de Fora, Instituto de Ciências Biológicas, Campus Universitário, CEP: 36036-900, Juiz de Fora, MG, Brazil; 3Laboratório de Ecologia Comportamental, Departamento de Zoologia, Universidade Federal de Juiz de Fora, Instituto de Ciências Biológicas, Campus Universitário, CEP: 36036-900, Juiz de Fora, MG, Brazil; 4Avèntures Sans Frontieres, BP 7248, Libreville, Gabon; 5Wildlife Conservation Society and Gabon Sea Turtle Partnership, BP 7847, Libreville, Gabon

Knowledge of mortality from natural events or anthropogenic conditions (Fossette et al. 2010). In Brazil, they are often seen at threats is important for the conservation of sea turtles. Stranding sea along the coast, with a higher concentration of individuals along surveys can provide important information on sea turtle distribution, the southern and southeastern coasts (Barata et al. 2004; Monteiro demography, and cause-specific mortality via collecting data and et al. 2016). The Brazilian nesting population for this species is biological samples from encountered carcasses (Chaloupka et al. restricted to a few individuals on the northern coast of Espírito 2008; Vélez-Rubio et al. 2013; Monteiro et al. 2016). In addition to Santo State (Thomé et al. 2007), although rare nesting has been the value for sea turtle status assessments, stranding data are useful observed in other locations along the coast (Barata & Fabiano 2002; for providing insights about anthropogenic interactions on sea turtle Bezerra et al. 2014). populations (Epperly et al. 1996; Casale et al. 2010). The International Union for the Conservation of Nature (IUCN) The term “unusual mortality event” (UME) is defined, according currently classify Dermochelys coriacea as Vulnerable, but in to the Marine Mammal Protection Act in U.S. national policy, Brazil, it is listed as Critically Endangered on the Brazilian list of as a stranding that is unexpected involving a significant die-off threatened species (Tiwari et al. 2013; MMA 2014). Major threats of any marine mammal population (NOAA 2015). Between the include incidental capture by industrial fisheries (Lewison et al. seven criteria that determine whether a mortality event is ‘unusual,’ it includes -24.500 ‘higher than expected numbers of stranded marine mammals in a given time and location’ (NOAA 2015). In this paper, we have also considered the -24.667 term UME for sea turtles, in view of a significant stranding of leatherback turtles that occurred mainly in October 2016, on the southern coast of São Paulo State, Brazil. -24.833 The leatherback turtle (Dermochelys coriacea) is the largest sea turtle species with a worldwide tropical and subtropical distribution (Eckert 2006). It is a highly pelagic animal that spends -25.000 most of its life in the open sea, feeding on jellyfish, salps, and other gelatinous organisms distributed in the water column (Marquez 1990). Houghton -25.167 et al. (2006) suggested that jellyfish aggregations are associated with leatherback distribution in the northeast Atlantic. Leatherback turtles are able to perform transoceanic migrations from reproductive to foraging zones and -48.167 -48.000 -47.833 -47.667 -47.500 -47.333 back (Benson et al. 2007), and also Figure 1. Study area located on the oceanic face of Ilha do Cardoso, Ilha Comprida and among Temporary Residence Areas Iguape, southern coast of São Paulo State, Brazil. The colored dots indicate stranding (TRAs) in neritic and oceanic domains locations of leatherback turtles according to sex from August 2015 to July 2017, a total according to multiple oceanographic of 20 individuals in Ilha Comprida, 5 in Iguape and 4 in Ilha do Cardoso.

Marine Turtle Newsletter No. 156, 2019 - Page 21 Figure 2. Dermochelys coriacea strandings from August 2015 to July 2017 in the study area.

2004; Fiedler et al. 2012) and destruction of coastal nesting habitats Each leatherback turtle was photographed, measured (curved (Pritchard 1996), and in the special case of the main nesting area for carapace length = CCL and total length = head to tail) and we Brazilian leatherback population next to Rio Doce Mouth in Espírito recorded date, latitude, longitude, tag numbers (if present), and Santo State, contamination due to the most serious environmental decomposition stage defined as COD 2 = freshly dead, COD 3 = disaster in Brazil, the Samarco mining waste dam collapse, that moderate decomposition, COD 4 = advanced decomposition and occurred in 2015 (Miranda &Marques 2016). High priority should COD 5 = mummified or only bone remains. We also recorded signs be placed on the monitoring of leatherback distribution, population of anthropogenic interactions. Necropsies of carcasses at CODs 2, levels and threats, as a way to continually assess the status of the 3 and 4 were performed to evaluate possible cause of death, sex species (IUCN/SSC 1995). According to multi-scale “regional identification, and samples were collected for histopathological, management units” (RMUs) (Wallace et al. 2010), the leatherback contaminant, and genetic analyses. turtle RMU in the SW Atlantic is considered in the High Risk Leatherback turtles were considered adult if CCL was larger - High Threat category, therefore, the most urgent conservation than the minimum size at the nearest nesting site in Espírito Santo: interventions are necessary in this region (Wallace et al. 2011); this 139 cm (Thomé et al. 2007). All the information was included in includes the Brazilian coast. the Aquatic Biota Monitoring System (SIMBA) and screened by a Here we report on an UME of leatherback turtles, which occurred filter tool to perform data analysis. in 2016, on the southeastern coast of Brazil, correlating the cause We recorded 29 dead stranded leatherback turtles between with biological, environmental and anthropogenic factors. The August 2015 and July 2017 in the study area; October 2016 was the results contribute to monitoring the status of the species in the South month with the highest stranding occurrence (n = 15), but the UME Atlantic in support of conservation efforts. began the previous month of September (n = 3) and continued into The study area is located on the southern coast of São Paulo early November 2016 (n = 4), with a total of 22 recorded stranded State, on the oceanic side of three islands: Iguape, Ilha Comprida turtles (Fig. 2). The mean size of leatherback turtles was CCL = and Ilha do Cardoso (Cananeia), a total of 136 km in length (Fig. 1). The highest rainfall rates occur from January to March, with a monthly average of 266.9 mm, while the lowest rates are recorded in July and August, with a monthly average of 95.3 mm (Silva 1989). From January to September, southwest winds predominate and, from October to December, the prevailing winds come from the east (Bergamo 2000). In the coastal region, wave trains predominate from the southeast quadrant, with a wave height of approximately 1 m (Araujo 2005). The residual tidal currents and the residual littoral transport of sediment act in the northeast direction, parallel to the coast (Picarelli et al. 2002). Leatherback turtle stranding data were obtained via daily beach surveys of Projeto de Monitoramento de Praias da Bacia de Santos (PMP-BS) conducted by Instituto de Pesquisas Cananeia (IPeC), from August 2015 to July 2017, along 100 km of Iguape, Ilha Comprida and Ilha do Cardoso. The PMP-BS is one of the conditions required by IBAMA as part of the environmental licensing process for oil and gas exploration, production and transport in the Pre- Figure3. Percentage of dead leatherback turtles according to Salt region (25.08333°S, 42.5833°W to 25.9167°S, 43.5667°W), decomposition stage. COD 2: n = 3; COD 3: n = 6; COD 4: between the isobaths of 2,100 - 2,300 m. n = 12; COD 5: n = 8 (see text for COD descriptions). Marine Turtle Newsletter No. 156, 2019 - Page 22 fishing effort during this period (Mendonça 2015). Monteiro et al. (2016) cited a mass-stranding event of 84 leatherback turtles recorded in November and December 2005 in Rio Grande do Sul, and associated the cause to unusual blooms of jellyfish that probably promoted a leatherback aggregation nearshore, thereby increasing the risk of bycatch in coastal fisheries. The same hypothesis may explain our observations. Jellyfish blooms also occurred during the period of leatherback UME in October 2016, as evidenced by large quantities of jellyfish washed ashore and recorded by beach surveys, mainly in Ilha Comprida, where the highest number of stranded leatherbacks was also recorded (n = 20/29). Both UMEs of leatherbacks in 2005 in Rio Grande do Sul and in 2016 in São Paulo occurred in La Niña years. This phenomenon usually increases winds from the southeast in the Southern Hemisphere (trade winds), that may have brought more jellyfish from oceanic to coastal waters, hence increasing the number of foraging leatherback turtles and the chances of incidental capture in fisheries, as seen in Monteiro et al. (2016). Leatherback distribution has previously been linked to jellyfish hotspots in the northeast Atlantic (Houghton et al. 2006) Figure 4. Male leatherback turtle (CCL = 144 cm) found in October 2016 at Ilha Comprida, SP, with linear cutaneous and TRAs corresponding to foraging areas all around the Atlantic marks on neck and flippers suggesting gill net entanglement. Ocean (Fossette et al. 2010), which corroborate the findings in our study. Considering that we recorded carcasses at COD 2 (n = 3) and COD 3 (n = 6) stages, it is assumed that at least these nine turtles 138.0 cm ± 17.2 SD, range: 98 - 171 cm (n = 17), and mean total died in nearshore waters, victims of bycatch in coastal fisheries. length = 186.1 cm ± 19.4 SD, range: 140 - 218 cm (n = 17). Eleven In fact, we recorded 11 individuals with anthropogenic interaction specimens were considered adults and six were subadults. Most of marks related to fishing activities, mainly gillnets. Kochet al. (2013) these animals were in the advanced decomposition stage, mainly verified that for turtle carcasses, there is a negative relationship COD 4 (n = 12) (Fig. 3). between distance from shore and likelihood of stranding on the Of the 29 individuals, 13 were males, five were females and 11 coast, and animals that die offshore may never strand. were of indeterminate sex due the advanced decomposition stage. Eckert (2006) proposed that movements of leatherback turtles Fig. 1 shows the location of each leatherback stranded according from one foraging area to another are driven by the opportunity to sex, within the study area. The female turtles were concentrated to forage in areas of distinct oceanic structure, which serve to further north in Ilha Comprida and Iguape, while males were concentrate their gelatinous prey (e.g., salps, Scyphomedusae, recorded along the three island coasts. Sex could not be determined Siphonophora) either at or below the surface. Fossette et al. for the majority of individuals distributed along Ilha do Cardoso (2010) identified nine TRAs in the neritic domain, confirming that and Ilha Comprida. leatherback turtles are also neritic foragers; the authors verified that On 22 October 2016, we found a dead leatherback turtle with a these TRAs were associated with mesoscale surface oceanographic flipper tag (ASF 14479) on Jureia beach, Iguape, São Paulo State, features of different types, such as altimetric features and/or Brazil (24.59°S and 47.28°W). The stranded carcass was severely surface chlorophyll a concentration (Fossette et al. 2010). Thus, decomposed (COD 4), measuring approximately 193 cm in total the oceanographic features of the southern coast of São Paulo length, from head to tail. This female leatherback turtle had been State influenced by La Niña in October 2016, provided conditions originally tagged on 23 November 2009 at Mayumba National for leatherbacks using the TRAs near the study area to forage on Park (3.75°S and 10.99°E) in southern Gabon, in the east Atlantic, jellyfish nearshore, becoming more susceptible to fishery bycatch measuring 142 cm (CCL), and was observed re-nesting on 21 and stranding. December 2009 on the same beach. The nesting season for leatherback turtles in the nearest nesting During beach surveys, unusual strandings of non-target fauna site in Espírito Santo to the study area (approximately 1,120 km of (other than marine birds, marine mammals and sea turtles) were distance) is from September to March, corroborating the presence also recorded. In October 2016, the same period of the UME of of mature adults during the UME in the study area. The turtles leatherback turtles, we also recorded unusual blooms of jellyfish could also have approached neritic waters possibly in the course (Scyphozoa) washed ashore, mainly in Ilha Comprida. Six of breeding or post-nesting migrations. Higher numbers of males leatherback turtles presented jellyfish and crustaceans in their (n = 13/29) than females (n = 5/29) suggest that females could be stomach contents. Out of 18 leatherback turtle carcasses necropsied, more concentrated northward near, the nesting areas in Espírito 11 presented signs of interaction with fishing gears (Fig. 4) and four Santo, possibly in their internesting internvals between clutch had ingested small amounts of plastic debris. deposition events. However, the female leatherback tagged in Gabon The highest number of leatherback strandings in October 2016 indicated that stranded individuals may belong to different Atlantic (n = 15/29), early austral spring, in the southern coast of São Paulo, populations. Fossette et al. (2010), in fact, showed that two satellite- could be explained by an association of important factors: jellyfish tagged individuals from different nesting populations (Southeast abundance and distribution, a La Niña event (NOAA 2016), and and Southwest Atlantic) used the same TRA, suggesting a potential Marine Turtle Newsletter No. 156, 2019 - Page 23 connection between turtles from both sides of the South Atlantic. ARAUJO, R.N. 2005. A propagação e deformação das ondas, a Billes et al. (2006) already presented evidence of leatherback dinâmica do transporte litorâneo e a evolução de linhas de costa em movement from Africa to Brazil reporting three females tagged localidades do litoral paulista. Tese (Doutorado em Engenharia), in Gabon between 2002 and 2003, recovered in southern and Escola Politécnica, Universidade de São Paulo, São Paulo. 148 pp. southeastern Brazil, after two years. The stranded female leatherback BARATA, P.C.R. & F.F.C. FABIANO. 2002. Evidence for tagged in Gabon in 2009 found in the present UME, was recaptured leatherback sea turtle (Dermochelys coriacea) nesting in Arraial after seven years, the longest interval recorded for the species on do Cabo, state of Rio de Janeiro, and a review of occasional Brazilian coasts. In addition to mark-recapture with metal tags and/or leatherback nests in Brazil. Marine Turtle Newsletter 96: 13-16. PIT tags, genetic analysis (Vargas et al. 2008) and satellite telemetry BARATA, P.C.R., E.H.S.M. LIMA, M. BORGES-MARTINS, J.T. (Fossette et al. 2010; Witt et al. 2011) also confirm the important SCALFONI, C. BELLINI & S. SICILIANO. 2004. Records of role played by the southern waters of South America for Gabon’s leatherback sea turtle (Dermochelys coriacea) on the Brazilian leatherback nesting population, the largest rookery for this species. Coast, 1969-2001. Journal of the Marine Biological Association Most stranded individuals observed were severely decomposed, of the United Kingdom 84: 1233-1240. making it impossible to determine the cause of death. However, BENSON, S.R., P.H. DUTTON, C. HITIPEUW, B. SAMBER, J. evidence of anthropogenic interactions was recorded, including BAKARBESSY & D. PARKER. 2007. Postnesting migrations of fishery bycatch and plastic debris. During the UME period, no leatherback turtles (Dermochelys coriacea) from Jamursba-Medi, “extraordinary” fishing effort occurred in the study area according Bird’s Head Peninsula, Indonesia. Chelonian Conservation & to local fisheries inspection institutions (personal communication Biology 6: 150-154. to the authors). Mendonça (2015) reported that the highest average BERGAMO, A.L. 2000. Características da hidrografia, circulação fish landing in the southern coast of São Paulo in 2010 was October e transporte de sal: Barra de Cananéia, Sul do Mar de Cananéia to February, overlapping with the UME period. We presume that e Baía do Trapandé. Dissertação (Mestrado em Oceanografia). jellyfish blooms initially aggregate leatherback turtles to forage, Instituto Oceanográfico, Universidade de São Paulo, São Paulo. increasing their vulnerability to capture by legal coastal fisheries. 118 pp. Plastic may easily be mistaken for jellyfish by leatherback turtles, BEZERRA, D.P., A.C.V. BONDIOLI, A.P.S. MAISTRO & M.B. potentially causing blockage of the gut (Mrosovsky et al. 2009). EBERT. 2014. Occasional leatherback turtle (Dermochelys In the present study, four individuals ingested non-lethal amounts coriacea) nests: First records in São Paulo State, Southeastern of plastic, which may potentially reduce the extent of the gut Brazil. Marine Turtle Newsletter 140: 6-8. from which absorption can occur and may well impair health and BILLES, A., J. FRETEY, B. VERHAGE, B. HUIJBREGTS, B. reproduction (Mrosovsky et al. 2009). GIFFONI, L. PROSDOCIMI, D.A. ALBAREDA, J.Y. GEORGES The UME of 22 leatherback turtles in September, October and & M. TIWARI. 2006. First evidence of leatherback movement early November 2016 on the southern coast of São Paulo State was from Africa to South America. Marine Turtle Newsletter 111: significant due to the current conservation status of the species. 13-14. Unusual blooms of jellyfish during that period were driven from CHALOUPKA, M., T.M. WORK, G.H. BALAZS, S.K.K. oceanic to shallow waters by the increase of SE trade winds caused MURAKAWA & R. MORRIS. 2008. Cause-specific temporal by La Niña, possibly attracting leatherback turtles to forage and and spatial trends in green sea turtle strandings in the Hawaiian increasing their risk of bycatch in coastal fisheries. The results of Archipelago (1982-2003). Marine Biology 154: 887-898. histopathological and contaminant analyses may contribute to a CASALE, P., M. AFRONTE, G. INSACCO, D. FREGGI, C. better explanatory diagnosis for this UME. VALLINI, P.P. D’ASTORE, R. BASSO, G. PAOLILLO, G. Understanding and investigating UMEs of threatened species ABBATE & R. ARGANO. 2010. Sea turtle strandings reveal high such as leatherback turtles is extremely important because they anthropogenic mortality in Italian Waters. Aquatic Conservation can serve as indicators of ocean health, giving insight into larger 20: 611-620. environmental issues. However, stranded carcasses represent a ECKERT, S.A. 2006. High-use oceanic areas for Atlantic minimum measure that usually does not exceed 10 - 20% of total leatherback sea turtles (Dermochelys coriacea) as identified at-sea mortality (Epperly et al. 1996; Koch et al. 2013), meaning using satellite telemetered location and dive information. Marine that many more turtles were probably dead at sea than the number Biology 149: 1257-1267. observed washed ashore. Contaminated food, plastic debris and EPPERLY, S.L., J. BRAUN, A.J. CHESTER, F.A. CROSS, J.V. overfishing are examples of main threats that this species and many MERRINER, P.A. TESTER & J.H. CHURCHILL. 1996. Beach others are facing. Conservation of highly migratory marine species strandings as an indicator of at-sea mortality of sea turtles. Bulletin such as Dermochelys coriacea requires international cooperation of Marine Science 59: 289-297. for implementation of transboundary management strategies to be FIEDLER, F.N., G. SALES, B.B. GIFFONI, E.L.A. MONTEIRO- truly effective. FILHO, E.R. SECCHI & L. BUGONI. 2012. Driftnet fishery Acknowledgments. We are grateful to the Instituto de Pesquisas threats sea turtles in the Atlantic Ocean. Biodiversity and Cananéia (IPeC) for logistics support. Sea turtle research in Conservation 21: 915-931. Gabon was carried out by Aventures Sans Frontieres and the FOSSETTE, S., C. GIRARD, M. LÓPEZ-MENDILAHARSU, P. Wildlife Conservation Society and is funded by the Marine Turtle MILLER, A. DOMINGO, D. EVANS, L. KELLE, V. PLOT, L. Conservation Fund (United States Fish and Wildlife Service, PROSDOCIMI, S. VERHAGE, P. GASPAR & J.Y. GEORGES. Department of the Interior). We are grateful to all the field teams 2010. Atlantic leatherback migratory paths and temporary involved in monitoring and tagging of Gabon’s nesting leatherbacks. residence areas. PLoS ONE 5 (11): e13908. Marine Turtle Newsletter No. 156, 2019 - Page 24 HOUGHTON, J.D.R, T.K. DOYLE, M.W. WILSON, J. PRITCHARD, P.C.H. 1996. Are the leatherbacks really threatened DAVENPORT & G.C. HAYS. 2006. Jellyfish aggregations with extinction? Chelonian Conservation & Biology 2: 303-306. and leatherback turtle foraging patterns in a temperate coastal SILVA, J.F. 1989. Dados climatológicos de Cananéia e Ubatuba environment. Ecology 87: 1967-1972. (Estado de São Paulo). Boletim Climatológico do Instituto IUCN/SSC. 1995. A global strategy for the conservation of marine Oceanográfico. 6: 1-21. turtles. Gland, Switzerland: IUCN/SSC. 25 pp. THOMÉ, J.C.A. C. BAPTISTOTTE, L.M.P. MOREIRA, J.T. KOCH, V., H. PECKHAM, A. MANCINI & T. EGUCHI. 2013. SCALFONI, A.P. ALMEIDA, D.B. RIETH & P.C.R. BARATA. Estimating at-sea mortality of marine turtles from stranding 2007. Nesting biology and conservation of the leatherback sea frequencies and drift experiments. PloS ONE 8 (2): e56776 turtle (Dermochelys coriacea) in the state of Espírito Santo, LEWINSON, R.L., S.A. FREEMAN & L.B. CROWDER. 2004. Brazil, 1988-1989 to 2003-2004. Chelonian Conservation & Quantifying the effects of fisheries on threatened species: the Biology 6: 15-27. impact of pelagic longlines on loggerhead and leatherback sea TIWARI, M., B.P. WALLACE & M. GIRONDOT. 2013. turtles. Ecology Letters 7: 221-231. Dermochelys coriacea (Southwest Atlantic Ocean MARQUEZ, R. 1990. FAO species catalogue; Sea turtles of the subpopulation). The IUCN Red List of Threatened Species world. An annotated and illustrated catalogue of the sea turtle 2013: e.T46967838A46967842. http://dx.doi.org/10.2305/IUCN. species known to date. FAO Fisheries Synopsis 125(11): 81pp. UK.2013-2.RLTS.T46967838A46967842.en. MENDONÇA, J. T. 2015. Caracterização da pesca artesanal no VARGAS, S.M., F.C. ARAÚJO, D.S. MONTEIRO, S.C. ESTIMA, litoral sul de São Paulo, Brasil. Boletim do Instituto de Pesca A.P. ALMEIDA, L.S. SOARES & F.R. SANTOS. 2008. Genetic 41: 479-492. diversity and origin of leatherback turtles (Dermochelys coriacea) MINISTÉRIO DO MEIO AMBIENTE (MMA). 2014. Lista de from the Brazilian coast. Journal of Heredity 99: 215-220. espécies da fauna brasileira ameaçadas de extinção. www.mma. VÉLEZ-RUBIO, G.M., A. ESTRADES, A. FALLABRINO & gov.br/biodiversidade/especies-ameacadas-de-extincao/fauna- J. TOMÁS. 2013. Marine turtle threats in Uruguayan waters: ameacada. Accessed on 12 January 2017. insights from 12 years of strandings data. Marine Biology 160: MIRANDA, L.S. & A.C. MARQUES. 2016. Hidden impacts of the 2797-2811. Samarco mining waste dam collapse to Brazilian marine fauna WALLACE, B.P., R.L. LEWISON, S.L. MCDONALD, R.K. - an example from the staurozoans (Cnidaria). Biota Neotropica MCDONALD, C.Y. KOT, S. KELEZ, R.K. BJORKLAND, E.M. 16: e20160169. FINKBEINER, S. HELMBRECHT & L.B. CROWDER. 2010. MONTEIRO, D.S., S.C. ESTIMA, T.B.R. GANDRA, A.P. SILVA, Global patterns of marine turtle bycatch. Conservation Letters L. BUGONI, Y. SWIMMER, J.A. SEMINOFF & E.R. SECCHI. 3: 131-142. 2016. Long-term spatial and temporal patterns of sea turtle WALLACE, B.P., A.D. DIMATTEO, A.B. BOLTEN, M.Y. strandings in Southern Brazil. Marine Biology 163: 247. CHALOUPKA, B.J. HUTCHINSON, F.A. ABREU-GROBOIS, MROSOVSKY N., G.D. RYAN & M.C. JAMES. 2009. Leatherback J.A. MORTIMER, J.A. SEMINOFF, D. 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Marine Turtle Newsletter No. 156, 2019 - Page 25 Rescue and Rehabilitation of Loggerhead Sea Turtles Caretta caretta from Dahanu Coast, Maharashtra, India

Prachi Hatkar, Dinesh Vinhenkar & Dhaval Kansara Wildlife Conservation & Animal Welfare Association (WCAWA), Dahanu Rd, Shringarpur, Dahanu, Maharashtra 401601, India (E-mail: [email protected], [email protected], [email protected])

Five species of sea turtles inhabit the Indian Ocean including, India. Conservation of sea turtles along the coast of Dahanu has been Dermochelys coriacea (leatherback turtle), Eretmochelys imbricata carried out by WCAWA (Wildlife Conservation and Animal Welfare (hawksbill turtle), Chelonia mydas (green turtle), Lepidochelys Association) along with the Dahanu forest division by rescuing and olivacea (olive ridley turtle) and Caretta caretta (loggerhead turtle) rehabilitating injured sea turtles since 2012. Dahanu was a major and all are reported along the Maharashtra coastline (Bhaskar 1984; nesting beach for olive ridley turtles and a minor nesting beach for Das 1985; Tikedar & Sharma 1985; Rajagopalan et al. 1996; Daniel green turtles (Shaikh 1984), where potential nesting beaches were 2002). These species of sea turtles are distributed widely all over also identified (Shaikh 1984). Beach patrols are currently being the world and face many anthropogenic threats (Chhapgar 2005). carried out by WCAWA in an effort to identify and record nesting Loggerhead turtles are rarely observed off the coast of mainland activity. India but the average size found along Indian Ocean coastlines are 74 No records of loggerhead turtles have been documented from cm (CCL), and 62 cm (CCW), and weigh about 69 kg. On average, the west coast in recent times as they are considered a non-nesting adult loggerheads weigh ~113.5 kg and have a curved carapace species in India (Kurian 2013). The exact foraging areas of the length of 91 cm (Venkatraman & Milton 2003). Their shell color loggerhead turtle in India are not known, but the maximum number is brown to reddish brown (Venkatraman & Milton 2003). Adult of foraging occurrences of this turtle has been reported from the and sub-adult loggerhead turtles are found primarily in subtropical southern Tamil Nadu coast and coral reef areas in the Gulf of Mannar (occasionally tropical) waters along the continental shelf and and Palk Bay (Tikader & Sharma 1985). Nesting apparently occurs estuaries of the Atlantic, Pacific and Indian Oceans (Venkatraman in Sri Lanka (Tripathy 2005). Four dead loggerhead turtles were & Milton 2003). Sexual maturity is estimated to be 25-35 years in reported from the Digha fish landing center and beach, West Bengal wild loggerheads (Chaloupka & Musick 1996). Most of the nesting in 1997 (Swapankumar 1997 a,b). zones of this turtle are in subtropical and temperate areas. The most A stranded sea turtle may be defined as any sea turtle found preferred habitat is the shallow continental shelf, and coastal bays dead, injured, sick or having tumors. One of the common causes for such as United States waters (Venkatraman & Milton 2003). They stranding is a buoyancy disorder. Floating turtles with a buoyancy are mainly carnivorous (Cardiff et al. 2012). Loggerhead turtles are disorder are unable to submerge and are either easily captured ‘Vulnerable’ and are listed on Appendix I of CITES and Appendices or blown ashore. They are also common victims of trauma due I and II of the (CMS) (Tikader & Sharma 1985). They are also to boat collisions or fishing gear entanglement. The trapping of protected by India’s Wildlife Protection Act, 1972 under Schedule I. intra-coelomic gas can be a cause of a buoyancy disorder. Gases Except for four dead loggerhead turtles reported from Tamil can also accumulate in a number of areas in the body (Shigenaka Nadu, there is no record available on sightings or nesting of this 2010). The appropriate treatment will vary based on the location species in India (Tripathy 2005). The State of Maharashtra plays of the trapped gas inside the turtle. Abnormal buoyancy may also an important role in the research and conservation of sea turtles in result from excessive gas in the gastrointestinal tract, sometimes,

Figure 1. Female loggerhead turtle rescued near Kelva Figure 2. Female loggerhead turtle rescued at Dahanu beach. beach. Marine Turtle Newsletter No. 156, 2019 - Page 26 Figure 3. Veterinarian examining a live stranded loggerhead Figure 4. Wounds on the rescued loggerhead turtle’s turtle. carapace and beak, along with eye infection. provoked by an obstructive lesion (RAC/SPA 2004). sampling the mucous around the eyes using swabs. If left untreated, A dead female sub-adult loggerhead turtle was retrieved from these infections can spread, cause blindness, and may kill the turtle. Dahanu beach on 5 June 2016 by WCAWA members. Morphometric The carapace was broken and necrosis (cell death) was evident. The measurements were not taken due to lack of equipment. carapace was also deformed with unnatural cuts on the marginal On 21 August 2017, an injured sub-adult female loggerhead turtle scutes for unidentified reasons. The carapace protects the turtle’s washed ashore at Dhakti Dahanu village. Another injured sub-adult internal organs and therefore severe strike wounds are often fatal. female was rescued 26 August 2017 by a local fisherman, near Kelva Deep wounds were observed on the carapace. Also the carapace was beach. After getting the rescue call, in both cases of live stranded covered with a layer of mud and muck. The turtle was cleaned of turtles, the WCAWA team rushed to the respective sites. Turtles external contaminants with a 10% Betadine solution. The dressing were picked up by the edges of the plastron and placed on a stretcher of the fractured carapace was done using Chlorhexidine spray for made of soft plastic. Then the turtles were brought to the center disinfection and cleaning of wounds. Maggots were found in the by ambulance. During transportation, the turtle’s carapaces were exposed wounds on the carapace along with rotting due to necrosis. covered with moist towels. Both turtles were administered similar An anti-maggot spray was applied to the affected area and maggots first aid treatment (Figs. 1-4). They were placed in isolation, in a tank were removed with the help of stainless steel tweezers. Necrotic and filled with seawater that had a filtration unit. Tanks were provided good tissues with cellular debris were cleaned on a regular basis. with artificial lighting. The water was replaced 3 to 4 times every Regular dressing of wounds was done with a local application of 12 hours. On these turtles, the carapaces, plastrons and beaks were honey and an aloe vera mixture with antiseptic creams smeared on infested with barnacles and their carapaces were decolorized. If all the wounds. Normal saline water diluted with the Enroflaxacine the barnacles present on a turtle are of a similar size and species, it injectable was used for flushing wounds to reduce infections. An may be an indication that the turtle was inactive for a period of time intra-coelomic injectable antibiotic Enrofloxacine and nonsteroidal (Shigenaka 2010). Barnacle infestation can reduce the speed and anti-inflammatory drug (NSAID) Meloxicam were given by the hydrodynamic shape of turtles. The exact age of both turtles was intracoelomic route. To counter dehydration, Ringers lactate and undetermined. Both of them were females; sex was determined by DNS was given intracoelomically every alternate five days. Epoxy the length of the tail (Table 1). Local anesthesia was administered plaster was applied temporarily to make the fracture site waterproof. prior to operating on the turtles. Barnacles were removed with the On every alternate day, epoxy plaster was replaced after the dressing help of a sterile stainless steel spatula. of wounds. In both cases, the injuries on the turtles were suspected to be In the second case, the turtle was weak and barely able to move its caused by boat or propeller strikes. No data on survival rates from body, it was infested with barnacles and parasites and the right fore boat strikes exist, however it is clear that many turtles die from the flipper was cut off completely. The turtle was kept in a freshwater trauma caused by the impact (Denkinger et al. 2013). In the first tank after its rescue. Changes in salinity and pH are thought to case, the damage to the turtle was clearly visible and evident, as help in the dislodging of external parasites. Buoyant turtles are not the strike had broken through the top of the turtle’s upper jaw considered releasable as they will have difficulty in foraging and are and carapace. The turtle was weak, dehydrated and the eyes were at high risk for watercraft collision. According to the veterinarian, watery. Treatment was carried out from the day following the rescue the chances of recovery and survival of the turtles were low due to operation. After conducting a medical examination it was confirmed critical injuries. These turtles were monitored closely since they were that the turtle had an eye infection. Asymmetrical swelling of the not fit to be released back into the water and might need permanent eye (that is one eye is puffed up but the other is not) is normally residence in a rehabilitation center. Their lungs were damaged and caused by physical damage. Eye infections are caused by a variety infected causing respiratory distress, so the turtles were kept in of bacteria most frequently Aeromonas and Pseudomonas species shallow water tanks with a continuous filtration system. Both turtles (http://www.seaturtleguardian.org). Due to the physical damage, a were hand fed with small pieces of Bombay duck and squids. Turtles secondary infection behind the eye can also cause a bulge. Further were dry docked for safety purposes. Dry docking is the practice investigation of a bacterial infection of the eye can be confirmed by of “forced basking,” which can aid the healing process by allowing Marine Turtle Newsletter No. 156, 2019 - Page 27 CL CW PL PW Weight Date Sex (cm) (cm) (cm) (cm) (kg) Rescue site Type of injury Maggot infection, 21.08.2017 F 74 55.5 57 57 46.4 Dahanu carapace broken 1 flipper missing, 26.08.2017 F 80.5 60.5 60.5 55.5 68.2 Kelva dehydrated 05.06.2016 F unk unk unk unk unk Dahanu Dead 16.01.1997 M 75 60 unk unk 55 Digha Landing center Dead 03.02.1997 M 83 58 unk unk 70 Digha beach Dead 03.02.1997 F 83 52 unk unk 75 Digha beach Dead 21.02.1997 M 58 40 unk unk 40 Digha beach Dead Average 75.6 54.3 n/a n/a 59.1 Max 83 60.5 n/a n/a 75 Min 58 40 n/a n/a 40 Table 1. Morphometric measurements of the rescued loggerhead turtles and previous records along the coast of Maharashtra, India. CL = carapace length, CW = carapace width, PL = plastron length, PW = plastron width. the skin and shell to dry resulting in a quicker wound recovery time Pvt. Ltd., team Abhijeet Jagtap, Amruta Dhamorikar, and Akshay (http://www.insectivore.co.uk/articles_turtles_how_to_dry_dock. Nachane for their valuable suggestions. Dipali Bandodkar and Dr. html). As per the attending veterinarian, the prognosis for both turtles S. Shivbala (IFS), Deputy Chief Conservator of Jawhar Division, was guarded as physical conditions were uncertain, and their health reviewed and improved the quality of the article. Sunil Belvekar could collapse at any time. Unfortunately, both rescued turtles died helped in image editing. in captivity due to lung infections on 8 October 2017. BHASKAR, S. 1984. The distribution and status of sea turtles in Boat strikes have been identified as an important mortality India. In: Silas, E.G. (Ed.). Proceedings of the Workshop on Sea factor in several nearshore turtle habitats worldwide (Denkinger Turtle Conservation. Central Marine Fisheries Research Institute, et al. 2013). Biological assessments of specific areas should be Kochi, Special Publication 18: 21-35. considered for designation of critical habitats for the threatened CARDIFF C., L. LOTTINO & T. MEINTJES. 2012. Loggerhead populations. There is an urgent need to assess turtle foraging areas Turtle Husbandry (2010) - An ORCA Foundation Initiative. 14 pp. near the Dahanu coast. In many cases, loggerhead foraging areas coincide with fishing zones (Denkinger et al. 2013). According to CHALOUPKA, M.Y. & J.A. MUSICK. 1996. Age, growth and Hazel et al. (2007) sea turtles cannot avoid boat collisions unless population dynamics. In: Lutz P.L. & J.A. Musick (Eds). The boats reduce their speed to 4 km/hr. Vessel Monitoring Systems Biology of Sea Turtles. CRC Press, Boca Raton. pp. 233-276. (VMS) should be implemented, which may help in controlling CHHAPGAR, B.F. 2005. Marine Life in India. Oxford University movements of cruise ships and could be applied for speed control Press, Oxford UK. 386 pp. on speedboats and outboard fishing boats during the nesting season DANIEL, J.C. 2002. The Book of Indian Reptiles. Bombay Natural from November to April in Maharashtra. Further, the Dahanu coast History Society & Oxford University Press, Mumbai. 238 pp. needs to be monitored for the identification of potential foraging DAS, I. 1985. Indian Turtles: A Field Guide. WWF-India, Calcutta, grounds. The knowledge gained from this research has helped India. 119 pp. the Dahanu forest department and WCAWA to develop protocols for wildlife rehabilitation. Further research is required to answer DENKINGER, J., M. PARRA, J. MUÑOZ, C. CONSTANZA, J.C. particular questions relating to parasites and bacterial infection and MURILLO, E. EDUARDO, F. RUBIANES & K. VOLKER. 2013. basic data like blood collection and analysis for health condition Are boat strikes a threat to sea turtles in the Galapagos Marine assessment in sea turtles are required for this region. Reserve? Ocean and Coastal Management 80: 29-35. Acknowledgments. Special thanks to all WCAWA members, HAZEL, J., I. LAWLER, H. MARSH & S. ROBSON. 2007. Boat volunteers and the Dahanu forest division members for their speed increases collision risk for the Green turtle Chelonia mydas. commitment to the care and treatment of wildlife casualties, without Endangered Species Research 3: 105-113. whom, much of the research discussed in this paper would not have KURIAN, A. 2013. Marine Turtles Along the Indian Coast: been possible. The authors thank the Dahanu and Maharashtra Forest Distribution, Status, Threats and Management Implications. Division for providing the opportunity to rescue and rehabilitate the WWF Report. 180 pp. injured sea turtles. The morphometric measurements were taken RAC/SPA. 2004. Guidelines to Improve the Involvement of Marine with calipers donated by Dr. R. Sureshkumar from the Wildlife Rescue Centres for Marine Turtles RAC/SPA, Tunis. 49 pp. Institute of India, Dehradun. The authors thank Terracon Ecotech RAJAGOPALAN, M.E., P. VIVEKANANDAN, S.K.M. SRINATH Marine Turtle Newsletter No. 156, 2019 - Page 28 & A.B. FERNANDO. 1996. Incidental catches of sea turtles Information Service Technical and Extension Series 148: 10. in India. Marine Fisheries Information Service Technical and SWAPAN, K., 1997b. On three dead turtles (Caretta caretta) Extension Series 143: 8-16. stranded at Digha, Midnapur district, West Bengal. Marine SHAIKH, A.K. 1984. Distribution of nesting sites of sea turtles in Fisheries Information Service Technical and Extension Series Maharashtra. In: Silas, E.G. (Ed.). Proceedings of the Workshop 149: 16. on Sea Turtle Conservation. Central Marine Fisheries Research TIKEDAR, B.K. & R.C. SHARMA. 1985. Handbook Indian Institute, Kochi, Special Publication 18: 109-116. Testudines. Zoological Survey of India, Calcutta. 156 pp. SHIGENAKA, G.. 2010. Oil and Sea Turtles: Biology, Planning TRIPATHY, B. 2005. Status of the loggerhead turtle in India. Current and Response. NOAA Report. 116 pp. Science 88: 535-536. SWAPAN, K. 1997a. On the incidental catch of pony fish Secutor VENKATRAMAN, K. & J.M.C. MILTON. 2003. Handbook Marine cantha indicator on the stranding of a Loggerhead turtle caught Turtles of India. Zoological Survey of India, Kolkata. 87 pp. at Digha, Midnapur district, West Bengal. Marine Fisheries

Marine Turtle Newsletter No. 156, 2019 - Page 29 A Juvenile Loggerhead Turtle (Caretta caretta) Tagged in Cuba Is Recaptured In Colombian Waters

Félix Moncada1, Cristian Ramírez-Gallego2, Juana Camero3, Marcos Gonzalez4, Gonzalo Nodarse5 & Karla G. Barrientos-Muñoz2,6 1Centro de Investigaciones Pesqueras, 248 No. 0603, e/5ª ave y mar, Santa Fe, Playa, La Habana, Cuba (E-mail: [email protected]); 2Fundación Tortugas del Mar, Carrera 46B # 43 sur 20 Int 402, Envigado, Antioquia, Colombia (E-mail: [email protected]); 3Hotel Punta Norte, Isla Tintipán, Archipiélago de San Bernardo, Bolívar, Colombia (E-mail: [email protected]); 4Parque Nacional Natural Corales del Rosario y de San Bernardo, Archipiélago de San Bernardo, Bolívar, Colombia (E-mail: [email protected]); 5Marina Marlin Cayo Largo, Isla de la Juventud, Cuba (Email: [email protected]); 6WIDECAST Colombia. Antioquia, Colombia (E-mail: [email protected])

A juvenile loggerhead (Caretta caretta) tagged in May 2017 at immediately; however, the turtle had a buoyancy disorder and was Cayo Largo (Canarreos Archipelago) Cuba, was recaptured at San subsequently taken to the marine turtle conservation program of Bernardo Archipelago, Colombia in June 2017 within the Corales the PNNCRySB, Punta Faro Hotel and Sueños de Mar Foundation del Rosario y de San Bernardo National Natural Park (PNNCRySB) on Isla de Múcura. (Fig. 1). The San Bernardo Archipelago has an area of 4.2 km2 and is part The loggerhead was tagged with a Monel tag (CB253) from of the PNNCRySB created in December 1996 by the Ministry of the tagging program of the Fisheries Research Center (CIP-Cuba), the Environment. It is located in the Colombian Caribbean, in its which has been tagging sea turtles since 1989 in different nesting and central region and consists of nine natural islands of coral origin feeding areas of the Cuban Archipelago; they also release hatchlings and one artificial island: Boquerón, Cabruna, Palma, Ceycén, Panda, from hatcheries that exist on the island. The loggerhead was tagged Múcura, Mangle, Maravilla, Tintipán, and an artificial island known by the staff of Marina Marlin (Cayo Largo) and released on 2 May as Santa Cruz (Díaz et al. 2000). 2017 from the hatchery located in Cayo Largo. The loggerhead was kept in rehabilitation for 39 days for Cayo Largo is located at the eastern end of the Canarreos observation. During this time, the buoyancy disorder was continually Archipelago. It is the most important nesting site for green and evaluated, until its subsequent release on 6 August under the loggerhead turtles in the Cuban Archipelago and one of the main bimonthly marine turtle release program led by the PNNCRySB. sites for green turtles in the Caribbean Sea (Medina et al. 2009; The loggerhead measured 50.5 cm curved carapace length (CCL) Nodarse et al. 2010). in Colombia, weighed 12.5 kg and was given an additional plastic The recaptured loggerhead came from a nest that hatched in tag with identification 577 on its front left flipper. September 2015 at Cayo Largo. A number of green and loggerhead The Marine Turtle Conservation Program was established 20 hatchlings are headstarted and kept in captivity in the Marine years ago to conserve marine turtles in the PNNCRySB, due to Turtle Rescue Center. Here, they are kept for one year or more the direct and incidental fishing of sea turtles in the area for many and are released before they reach two years of age. Upon release, years. The fishermen in the area were unaware of their current the loggerhead of interest for this report measured 50 cm curved conservation status and local threats. Initially, the program was carapace length (CCL) and weighed 13.5 kg. directed exclusively to the area of the Rosario Archipelago. In On 29 June 2017, loggerhead CB253 was recaptured within the 2015, in support of the Punta Faro Hotel and the Sueños de Mar San Bernardo Archipelago on Tintipán Island by the staff of the Foundation, the Marine Turtle Protection Program was created in the Punta Norte Hotel. These individuals attempted to release the turtle San Bernardo Archipelago. There, the fishermen deliver the turtles

Figure 1. Geographic location of Cayo Largo (Cuba) and San Bernardo Archipelago, Colombia Colombia. Marine Turtle Newsletter No. 156, 2019 - Page 30 that they capture to hotel staff, where they remain for approximately (Punta Faro Hotel) who were crucial in the process of data collection, two months in a natural swimming pool under the supervision of care, and subsequent release of the turtle. The authors thank Dr. trained personnel of the local national parks. Releases are conducted Karen L. Eckert (WIDECAST) and the late Peter Eliazar of the with local community children under the environmental education Archie Carr Center for Sea Turtle Research (ACCSTR) including program for the conservation of key species within the territory (TN the CMTTP (Cooperative Marine Turtle Tagging Program) for Stephanie Pauwels, personal communication, 12 December 2017). their support in the quick and timely search for information. Lastly, The time between the initial date of release and the date of we thank Sarah Hirsch and Dr. Justin Perrault and of Loggerhead recapture was 59 days. Therefore, we can estimate that the turtle Marinelife Center, Florida for helping us improve the quality of traveled between the Cuban Archipelago and the San Bernardo this manuscript. Archipelago in Colombia in a very short time. It is important to note AMAYA-ESPINEL, J.D. & L.A. ZAPATA. 2014. Guía de that other species of sea turtles tagged in the Cuban Archipelago, las especies migratorias de la biodiversidad en Colombia. such as the hawksbill turtle (Eretmochelys imbricata), have been Insectos, murciélagos, tortugas marinas, mamíferos marinos recaptured in Colombian waters (e.g., a satellite-tagged nesting y dulceacuícolas. Vol. 3. Ministerio de Ambiente y Desarrollo female and a juvenile specimen tagged with a metallic tag were both Sostenible / WWF-Colombia. Bogotá, D. C., Colombia. 370 pp. recaptured in this area; Moncada et al. 2012). It is apparent that the BARRIENTOS-MUÑOZ, KG., C. RAMÍREZ-GALLEGO & V. area of the Colombian Caribbean could be a destination area for PÁEZ. 2015. Tortuga carey. Eretmochelys imbricata (Linnaeus, turtles in different life stages traveling from Cuba. 1766). In: Morales-Betancourt, M.A., C.A. Lasso, V.P. Páez & The San Bernardo Archipelago serves as an important nesting B. Bock (Eds.). Libro Rojo de Reptiles de Colombia (2015). and/or feeding area for sea turtles in the Colombian Caribbean, Instituto de Investigación de Recursos Biológicos Alexander von due to the presence of coral reefs, seagrasses and sandy beaches Humboldt, Universidad de Antioquia, Bogotá, D.C., Colombia. (Rincón-Diaz & Rodríguez-Zarate 2004). Studies have shown that pp. 127-131. juvenile, subadult, and adult hawksbill and green turtles (Chelonia mydas) are primarily present; most of the evidence of the presence of CEBALLOS-FONSECA, C.P. 2004. Distribución de playas de loggerhead turtles in the area comes from local fishermen (Ceballos- anidación y áreas de alimentación de tortugas marinas y sus Fonseca 2004). amenazas en el Caribe colombiano. Boletín de Investigaciones This record is important for the contribution of knowledge of the Marinas y Costeras 33: 79-99. loggerhead turtle in the Greater Caribbean, but also essential for DIAZ, J.M., L.M. BARRIOS, M.H. CENDALES, J. GARZÓN- knowledge of the species in Colombia. Worldwide, the loggerhead FERREIRA, J. GEISTER, M. LÓPEZ-VICTORIA, G.H. turtle is categorized as Vulnerable according to the IUCN (2017). OSPINA, F. PARRA-VALENDIA, J. PINZÓN, B. VARGAS- In Colombia, according to the Red Book of Reptiles of Colombia ANGEL, F.A. ZAPATA & S. ZEA. 2000. Áreas coralinas (2015) it is categorized as Critically Endangered, being one of de Colombia. INVEMAR, Santa Marta, Serie Publicaciones the three species, of the five species present in the country, with Especiales No. 5, 176 pp. the highest risk of extinction as well as the hawksbill turtle (E. KAUFMANN, R. 1973. Biología de las tortugas marinas Caretta imbricata) and the leatherback turtle (Dermochelys coriacea) caretta y Dermochelys coriacea, de la costa Atlántica colombiana. due mainly to the consumption of their eggs and meat in adults, Revista de la Academia Colombiana de Ciencias Exactas, Físicas subadults and juveniles (Barrientos-Muñoz et al. 2015; Páez et al. y Naturales 14: 67-80. 2015; Ramírez-Gallego et al. 2015). MEDINA, Y., F. MONCADA & G. NODARSE. 2009. Anidación In Colombia, loggerhead turtles have the highest risk of local de la tortuga verde (Chelonia mydas) y caracterización de las extinction (Amaya-Espinel & Zapata 2014; Páez et al. 2015). playas en Cayo Largo, Cuba. Revista Cubana de Investigaciones Kaufmann (1973) and Tufts (1973) estimated that more than 400 Pesqueras 26: 66-72. females nest annually in the old Buritaca Reserve, with an additional 600 females/year nesting at Buritaca Beaches in Don Diego and MONCADA, F., G. NODARSE, Y. MEDINA & E. ESCOBAR. Quintana, Department of Magdalena (Ceballos-Fonseca 2004). At 2012. Distribution, size composition and growth of immature present there are no sites in Colombia with more than six nests per hawksbill turtles (E. imbricata) in the Jardines de la Reina season (Páez et al. 2015). archipelago, Cuba. In: T.T. Jones & B.P. Wallace (Comps.). st Our report provides valuable information regarding the migratory Proceedings of the 31 International Sea Turtle Symposium. behavior, habitat use, and time of displacement of highly migratory NOAA Tech Memo NMFS-SEFSC-631. p. 235. species such as sea turtles, as well as the importance of regional MONCADA, F., L.A. HAWKES, M.R. FISH, B.J. GODLEY, efforts for conservation and management of sea turtles in the Greater S.C. MANOLIS, Y. MEDINA, G. NODARSE & G. WEBB. Caribbean. 2012. Patterns of dispersal of hawksbill turtles from the Cuban Acknowledgments. We thank the Staff of Marina Marlin (Cayo shelf inform scale of conservation and management. Biological Largo) who have been tagging Cayo Largo sea turtles for years. We Conservation 148: 191-199. also thank Miguel Angel de Hoyos Camero and the staff of Punta NODARSE, G., F. MONCADA, Y. MEDINA, C. RODRÍGUEZ, Norte Hotel for the rescue of the turtle and subsequent delivery to F. HERNÁNDEZ, R. BLANCO & E. ESCOBAR. 2010. the Marine Turtle Conservation Program in the area. Special thanks Comportamiento de la anidación de tortugas marinas en los Cayos to the Chief of the Protected Area TN Stephanie Pauwels, Jorge San Felipe y Archipiélago de los Canarreos, Cuba (2001-2006). Moreno, and Guido Lopez who serve as officials of the PNNCRySB; Revista Cubana de Investigaciones Pesqueras 27: 67-71. Alejandro Alzate (Sueños de Mar Foundation) and Oscar Alzate Marine Turtle Newsletter No. 156, 2019 - Page 31 PÁEZ, V., C. RAMÍREZ-GALLEGO., K.G. BARRIENTOS- RINCÓN-DÍAZ, M.P. & C.J. RODRÍGUEZ-ZARATE. 2004. MUÑOZ. 2015. Tortuga caguama. Caretta caretta (Linnaeus, Caracterización de playas de anidación y zonas de alimentación 1758). In: Morales-Betancourt, M.A., C.A. Lasso, V.P. Páez & de tortugas marinas en el archipiélago de San Bernardo, Caribe B. Bock (Eds.). Libro Rojo de Reptiles de Colombia (2015). colombiano. Boletin de Investigaciones Marinas y Costeras 33: Instituto de Investigación de Recursos Biológicos Alexander von 137-158. Humboldt, Universidad de Antioquia, Bogotá, D.C., Colombia. TUFTS, C.E. 1973. Report on the Butitaca Marine Turtle Nesting pp. 118-121. Reserve with Emphasis on Biological Data from “Operation RAMÍREZ-GALLEGO, C., V. PÁEZ & K.G. BARRIENTOS- Tortuga 1972” and Recommendations for the Future. Report for MUÑOZ. 2015. Tortuga caná. Dermochelys coriacea (Vandelli, Inderena-Cuerpo de Paz. Bogotá, D.F., Colombia. 73 pp. 1761). In: Morales-Betancourt, M.A., C.A. Lasso, V.P. Páez & B. Bock (Eds.). Libro Rojo de Reptiles de Colombia (2015). Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Universidad de Antioquia, Bogotá, D.C., Colombia. pp. 122-126.

Marine Turtle Newsletter No. 156, 2019 - Page 32 Using Bamboo Nest Covers to Prevent Predation on Sea Turtle Eggs

Emma Korein1, Alba Caballol2, Pascall Lovell1, Laura Exley1, Carlos Porras Marin3, José Carillo3, Grace Bond1, Loris Capria1, Samantha Earl1, Olivia M. Ferrari1, Joseph Hamm1, Sarah Johnson-Gutierrez1, Courtney King2, Atenea Malmierca2, Laura McAnally1, Ellen Price1, Ellen Riddick1 & Lauren Stokes1

1Frontier, 50-52 Rivington St, London EC2A 3QP, UK (E-mail: [email protected]; [email protected]; costarica. [email protected]; [email protected]; [email protected]; [email protected]; [email protected]; joseph.hamm@ hotmail.com; [email protected]; [email protected]; [email protected]; [email protected]; [email protected]); 2Planet Conservation, Puerto Viejo de Talamanca, 70403, Costa Rica, (E-mail: [email protected]; [email protected], [email protected]); 3COTORCO, Puerto Jimenéz, Golfito, 60702 Costa Rica (E-mail: cotorco@ adicorcovado.org)

Predation on sea turtle eggs poses a serious threat to turtle thoughtful and deliberate planning and should be tailored to the populations. Accounts of predation are widespread and include specific predators in a region (Isakssonet al. 2007; O’Connor et al. a range of predators (Fowler 1979; Broderick & Godley 1996; 2017). Additionally, nest covers designed in previous studies have Whiting & Whiting 2011; Kurz et al. 2012; Burger & Gochfeld been described as having certain disadvantages, including being 2014; Ruiz-Izaguirre et al. 2015; Lei & Booth 2017; O’Connor et expensive, heavy, challenging or time consuming to place on nests, al. 2017). While a certain degree of predation on sea turtle eggs is and being fully enclosed such that hatchlings cannot crawl freely normal, domestic and stray dogs have increased predation rates to to sea without human intervention (Lei & Booth 2017; O’Connor unnatural levels (Fowler 1979; Broderick & Godley 1996; Burger et al. 2017). It is therefore important to understand the practicality & Gochfeld 2014; Ruiz-Izaguirre et al. 2015). of a nest cover design when determining its overall effectiveness A number of strategies have been attempted to reduce predation as a conservation tool. on sea turtle nests, including lethal removal of the predator Our study has two central aims: 1) to determine the rate of (Ratnaswamy et al. 1997; O’Connor et al. 2017), taste aversion predation, seasonal predation patterns, and identify the predator conditioning (Ratnaswamy et al. 1997), placement of chili powder species of sea turtle nests on Playa Carate, Costa Rica, and 2) to or habanero pepper around a nest (Lamarre-DeJesus & Griffin 2015; test the effectiveness and practicality of bamboo nest covers as a Lei & Booth 2017), and a cage or nest cover to prevent animals from method of preventing predation on sea turtle eggs. accessing the nest (Broderick & Godley 1996; Ratnaswamy et al. Playa Carate is a 2.6 km long sea turtle nesting beach situated on 1997; Ali & Ibrahim 2002; Kurz et al. 2012; Lei & Booth 2017; the Osa Peninsula on the South Pacific coast of Costa Rica (between O’Connor et al. 2017). Out of all these methods, the use of a nest 8.436333 °N, -83.440139 °W and 8.442367 °N, 83.462083 °W). cover is frequently cited as the most effective predation prevention The most common sea turtle nesting on this beach is the olive strategy (Ratnaswamy et al. 1997; Kurz et al. 2012; Lei & Booth ridley turtle (Lepidochelys olivacea), followed by the Pacific green 2017; O’Connor et al. 2017). For example, O’Connor et al. (2017) turtle (Chelonia mydas). Hawksbill (Eretmochelys imbricata) and found that controlling hunting foxes via lethal removal resulted leatherback (Dermochelys coriacea) turtles also nest on this beach, in a 27% predation rate on sea turtle eggs, while the use of nest though rarely. In the past few decades, this region has undergone covers reduced the predation rate to 3%. However, nest covers that considerable development due to a rise in the tourism and gold are not properly implemented can be ineffective, or in the worst- mining industries (Minca & Linda 2000). Carate has attracted a case scenario can actually attract predators that learn to associate sizeable resident population despite the remoteness of the area, a nest cover with incubating eggs (Niehaus et al. 2004; Isaksson resulting in a relatively large population of both domestic and et al. 2007). The use and design of nest covers therefore requires stray dogs. Being situated adjacent to Corcovado National Park,

Figure 1. Left photo: a bamboo nest cover with pieces woven together and tied with hessian twine. Right photo: a bamboo nest cover secured in the sand by anchoring sticks into each corner and burying the edges of the cage in sand. Marine Turtle Newsletter No. 156, 2019 - Page 33 this region is also highly biodiverse and inhabited by a number and presence/absence of a bamboo cover. Predator species was of predatory animals that extend their hunting range beyond park determined based on visual confirmation of the animal or animal boundaries and onto beach habitats (Kappelle 2016). footprints near the nest. The one exception was predation by crabs, Surveys were conducted every morning from 1 May 2017 until which was recorded when an egg shell was empty with one small slit 30 April 2018 by a trained employee of one of three sea turtle in the shell where the crab claw struck. The egg shells were counted research and conservation organizations in this region: Frontier, to estimate the number of eggs that were predated. Broken shells Planet Conservation, and COTORCO. From May to December were counted as a whole egg if more than 50% of the shell was intact. 2017, when the number of nesting turtles was highest, patrols were If the nest was only partially predated, the remaining surviving also conducted every night at mid-tide between 19:00 and 23:00. eggs were reburied in the chamber and the predated fragments were To minimize the disturbance of night patrols on nesting females, buried elsewhere. If a bamboo cover had not already been over the survey teams were limited to six people and only red lights were nest but was placed on after predation, this was noted in the data. used. Both morning and night patrols consisted of walking the All statistical analyses were conducted using Microsoft Excel length of the beach looking for the presence of adult turtle tracks Version 1806 and RStudio Version 1.1.463. A generalized linear and predated nests. model (GLM) with a binomial error structure was calculated to test When an adult turtle track was encountered, the following whether there was a significant relationship between a nest having a information was recorded: date, time, species, presence or absence bamboo cover and the likelihood of it being predated. A result was of a nest, whether a bamboo cover was placed on the nest, and considered statistically significant if p≤0.05. The risk ratio with 95% nest location. The presence of a nest was determined by carefully confidence intervals was also calculated to determine the relative inserting a stick into the sand to locate the egg chamber, indicated probability of a nest being predated with versus without a nest by a marked change in resistance. If no egg chamber was detected, cover. A risk ratio of 1 would indicate no difference in probability the track was marked as a “false crawl.” The species of turtle was of predation across the two conditions, so a result was considered verified either visually if encountered during night patrol or by the statistically significant if the confidence interval did not straddle 1. size and symmetry of the tracks of the nesting crawl. During the study period 1,032 new nests were found on Playa The beach was divided into numbered sectors, marked by a Carate. Nineteen of the nests were identified as laid by Pacific green painted wooden post every 25 m. Nest location was assigned by the sea turtles, one was identified as laid by a hawksbill sea turtle, and sector in which the nest was found. Bamboo covers were distributed the remaining 1,012 nests were identified as laid by olive ridley sea at sector posts along the beach and used opportunistically whenever turtles. Another 277 false crawls were recorded, which included a cover was available. Every new nest was assigned a nest number one leatherback turtle, 12 Pacific green turtles, and 264 olive ridley and given a marked wooden block tied to a stick placed one meter turtles. behind the nest or in the top right corner of a bamboo nest cover. Of the 1,032 nests found, 79 were relocated to a hatchery, 56 Bamboo nest covers were constructed by placing strips of bamboo were poached the same night they were laid, and 6 were washed approximately 1 m in length in a 7x7 grid formation (Fig. 1). Each away by the sea immediately after being laid, leaving a total of 891 strip was placed approximately 10 cm apart, a gap that was wide nests that could be subject to predation during the nesting season enough for hatchlings to emerge through the cover but narrow (including 39 nests that were relocated from one section of the beach enough to inhibit digging by predators. If softer, more recently cut to another). Out of these 891 nests, 133 experienced some level of bamboo was used, the strips could be secured in place by weaving predation over the course of the study, resulting in a predation rate them together. If older, less malleable bamboo was used, the pieces of 14.9%. An additional 74 unmarked nests were also found to be were tied together using plastic or hessian twine. Nest covers were predated throughout the season. A nest could have been unmarked placed directly on top of turtle nests and secured in place by digging either because the number label fell off or because surveyors had a sturdy stick into each corner and burying the cover in sand. not seen the tracks after a nest was laid. The unmarked nests were New nest covers were made at the beginning of each week, not included in predation rate calculations, although these data requiring between 10 - 20 minutes each to construct. Covers that contributed to our understanding of the active predators on Playa were broken or washed by the tide to another area of the beach were Carate. The average number of eggs predated per nest was 46.7. The collected for repair. Intact covers could be reused on subsequently average clutch size of olive ridley turtles at Playa Carate was 88.9 laid nests. Nest covers were stored in piles along the beach so that eggs per nest, based on 115 relocated nests that did not experience a nest in any given sector could be protected when a cover was predation before relocation. available. Three predated nests were green turtle nests and the rest were Predated nests were identified based on the presence of animal olive ridley nests. Two of the predated green turtle nests, as well as prints, signs of digging (soft, recently disturbed sand), and the 46 olive ridley nests, were predated the same night they were laid. presence of broken or shredded egg shells on the surface of the The remaining nests were predated on average 40 days after being sand in close proximity to the nest. Only freshly predated nests laid. Olive ridley hatchlings tend to emerge 45-55 days after the eggs were recorded, as animals would often dig up previously predated are laid (Maulany et al. 2012; Honarvar et al. 2016), meaning that or hatched nests for which data had already been recorded. A nest nests were often predated close to the time of expected hatchling was identified as freshly predated based on the color and texture of emergence. Peak nesting season occurred from July to August 2017 the egg shells; newly predated eggs were soft and white, while old and from November 2017 to January 2018 (Table 1). The highest eggs were dried out and had a yellow tint. number of predations also occurred within these months, as well When a newly predated nest was found, we recorded the as in September 2017. Predation rate for the month was defined as date, time, nest location (sector), nest number, predator species, nests predated divided by total nests laid that month and was highest

Marine Turtle Newsletter No. 156, 2019 - Page 34 Month Nests laid Nests predated Predation rate Average number May 2017 5 1 20.0% Nests % total nests eggs predated per Jun 2017 40 9 22.5% Species predated predated nest (min, max) Jul 2017 120 19 15.8% Dogs 54 26.1% 50.6 (8,107) Aug 2017 202 33 16.3% Crabs 52 25.1% 2.6 (1,15) Birds of Sep 2017 46 20 43.5% 48 23.2% 50.4 (10, 107) Prey Oct 2017 39 8 20.5% Racoons 3 1.4% 58 (53,61) Nov 2017 197 38 19.3% Table 2. Quantity and percentage (out of all 207 predated Dec 2017 120 11 9.2% nests) of nests predated by each identified predator, as well Jan 2018 72 15 20.8% as the average, minimum, and maximum number of eggs Feb 2018 18 3 16.7% predated per nest by each identified predator. Mar 2018 21 1 4.8% regions of Costa Rica (Wainwright 2007) and have been observed Apr 2018 11 1 9.1% predating nests on beaches adjacent to Playa Carate (Korein, E. unpubl. data). We hypothesize that the high number of dogs on Table 1. Number of sea turtle nests laid, and number of nests Carate scare the coatis and racoons from this beach. predated each month of the study period. Predation rate = the number of nests predated in a given month divided by the Previous studies reported that vultures scavenged turtle nests number of nests laid that month x 100. that had been dug up by another animal, rather than digging up a nest themselves (Burger & Gochfeld 2014). In our study, most nests in September 2017 by a large margin - nearly double that of the predated by vultures also had dog prints present, suggesting that second highest predation rate. While relatively few nests were laid a dog could have dug up the nest first. However, there were other in September, there were many nests laid in the months leading up nests for which only bird prints were found. Anecdotally, surveyors to it. We suspect that predators became habituated to finding food reported seeing crested caracaras actively digging up nests, while on the beach and continued to hunt frequently in September, thus vultures were most often seen eating eggs already on or near to the increasing the predation rate. The predation rate was also relatively surface. Black hawks were only seen consuming hatchlings as they high in some of the quieter nesting months, such as May and June were walking to sea, rather than predating eggs from a nest. 2017. Bamboo nest covers should therefore be used all year round Dogs were the most frequently reported predator of turtle when possible, rather than just in the peak nesting season. nests. We suggest managing predation by dogs to be the highest Out of the 207 recorded predated nests (both marked and conservation priority because dogs have been anthropogenically unmarked), 123 (59.4%) predators were identified. Multiple introduced to this area and therefore do not play a natural role in the predators were identified for 29 nests, with birds of prey and dogs local food chain. Interestingly, the presence of dogs may scare away having the most overlap (28 nests). When multiple predators were more natural predators to turtle eggs, such as coatis and racoons. identified, it was not possible to distinguish how many eggs were Therefore, we sought to protect nests from dogs through the use of predated by each type of predator. This may explain partially why bamboo nest covers, rather than control numbers of dogs directly. birds and dogs appeared to predate a similar number of eggs per Throughout the season 213 bamboo nest covers were placed over nest, as dogs and birds were commonly found predating the same newly laid nests. For calculating the effectiveness of bamboo nest nests. In cases where the specific bird of prey could be identified covers at preventing predation, we excluded nests predated solely (the bird itself was seen rather than just footprints), the majority of by crabs, because crabs dig into nests under the sand and cannot be bird predators were black vultures (Coragyps atratus) and turkey stopped by bamboo nest covers. Of the nests with bamboo covers, 14 vultures (Cathartes aura). Less commonly, crested caracaras (6.6%) were predated. The predators of these nests were identified (Caracara cheriway) and black hawks (Buteogallus subtilis) were as either dogs, birds, racoons, or a combination of the three. Eight also found predating nests. of these nests did not have a nest cover at the time that the surveyor The data suggest that dogs and birds of prey caused the most found and collected predation data from the nest. We suspect overall damage to turtle nests (Table 2). This is consistent with that the bamboo cover was washed away by the tide or extreme several previous studies based in Costa Rica, which also reported weather (heavy rains and winds), exposing the nest to predators. In dogs and vultures were the most prominent predators of both green the remaining 6 cases, the animal had managed to either push the and olive ridley nests (Fowler 1979; Burger & Gochfeld 2014). bamboo cover to the side or dig around and then under the nest cover. While crabs predated a significant number of nests, they tended to In contrast, out of the remaining 678 nests that did not have only predate a few eggs at a time and therefore the damage they bamboo nest covers, 119 (17.6%) were predated. A generalized caused to turtle populations was relatively low. Raccoons (Procyon linear model (GLM) with a binomial error structure revealed cancrivorus or Procyon lotor) were identified as predators of turtle that nests without a bamboo cover were significantly more likely to nests, though relatively infrequently compared to dogs and birds. be predated than nests with a bamboo cover (Table 3). A calculation White-nosed coatis (Nasua narica) were not identified as a predator of the risk ratio found that the probability of a nest being predated on any occasion in our study. This was unexpected, as coatis are without a bamboo nest cover was 2.49 (95% CI: 1.50 - 4.15) times reported to be the primary predator of olive ridley nests in some greater than the probability of predation with a nest cover. There Marine Turtle Newsletter No. 156, 2019 - Page 35 Standard Confidence Intervals Estimate Error 2.5% 97.5% z-value Pr(>|t|) (Intercept) -2.65 0.28 -3.24 -2.15 -9.6 No bamboo 1.11 0.29 0.56 1.73 3.76 < 0.001 Table 2. Outputs for the estimates, standard errors, confidence intervals, z-values and p-values of the coefficients for the generalized linear model describing the effect of bamboo nest covers on predation. These outputs are reported in the logistic scale, as a binomial error structure was applied for the GLM. “No bamboo” is a categorical variable representing nests that did not have bamboo covers on them, while the intercept represents the variable where nests did have covers on them. The result was considered statistically significant (p<0.001). were 8 cases when an uncovered nest was partially predated, and year round. The most successful bamboo covers use hessian rather then surveyors placed a bamboo nest cover on top of the remaining than plastic twine, are made from weaving freshly cut bamboo pieces surviving eggs. None of these nests were predated subsequently. together, and are secured into the sand with anchoring sticks in each Our data show that bamboo nest covers can reduce the rate corner. Depending on the resources available, nesting beaches in of predation on incubating sea turtle eggs. Nest cover designs other regions around the world could use bamboo nest covers as a described in previous studies have harbored certain disadvantages, method of reducing predation on turtle eggs. such as being expensive, heavy, difficult to carry long distances, Acknowledgements. We acknowledge the hard work and challenging or time consuming to install, or being fully enclosed commitment of the staff, volunteers and interns of Frontier, Planet such that hatching turtles cannot pass the physical barrier of the Conservation and COTORCO. We give special recognition to cover to make their way to sea (Lei & Booth 2017; O’Connor et the following individuals who significantly contributed to data al. 2017). The bamboo nest covers used in this study were sturdy, collection and entry: Nina Cristiano, Jorge Cubillo, Iain Dobson, lightweight and easy to move, simple to construct, inexpensive, and Tom Everley, Annabell Field, Neil Garry, Bella Jack, Enoc Jimenez allow hatchlings to emerge and walk to sea without being blocked by Arias, Emma Johnstone, Jordan Leizert, Aoife Luscombe, Loreta the nest cover, making them an efficient and cost-effective predation Mikulyte, Ewan Quayle, Nicola Scott, Rebecca Sexton, Anjlie prevention system that is well suited to this region of Costa Rica. Shah, Tamara Spivey, Ella Wilkinson. Permits were distributed by Our data revealed that nests were often predated just before the Ministerio de Ambiente y Energía (MINAE) to Katya Barrantes, typical time of hatching for olive ridley nests. This emphasizes the the lead biologist of COTORCO. importance of having a nest cover design that allows hatchlings to ALI, A. & K. IBRAHIM. 2002. Crab predation on green turtle leave the nest without being obstructed by the cover, eliminating (Chelonia mydas) eggs incubated on a natural beach and in turtle the need to remove the cover and risk predation prior to hatching. hatcheries. In: Arai, N. (Ed.). Proceedings of the 3rd Workshop An additional benefit of bamboo nest covers is that they are more on SEASTAR2000. Graduate School of Informatics, Kyoto environmentally friendly than cover designs made entirely of plastic; University, Japan. pp. 95-100. this is especially true when hessian twine is used to tie bamboo BOUCHARD, S. & K. BJORNDAL. 2000. Sea turtles as biological pieces together rather than plastic twine. Should a bamboo cover be transporters of nutrients and energy from marine to terrestrial washed out by tides, only natural and biodegradable materials are at ecosystems. Ecology 81: 2305-2313. risk of entering the sea, rather than contributing to the burgeoning level of plastic debris in the ocean that can have detrimental effects BRODERICK, A.C. & B.J. GODLEY. 1996. Population and nesting on sea turtle health (Nelms et al. 2015). ecology of the green turtle, Chelonia mydas, and the loggerhead There were some disadvantages to the bamboo nest cover design. turtle, Caretta caretta, in northern Cyprus. Zoology in the Middle Bamboo nest covers are time consuming to construct (approximately East 13: 27-46. 10-20 minutes per cover), and mass production of them requires a BURGER, J. & M. GOCHFELD. 2014. Avian predation on olive team of people. High tides can dislodge bamboo covers and move ridley (Lepidochelys olivacea) sea turtle eggs and hatchlings: them to other locations on the beach or drag them into the water, avian opportunities, turtle avoidance, and human protection. emphasizing the need to anchor covers into the sand with deeply Copeia 2014: 109-122. buried sticks. Thin bamboo strips are prone to breaking if treated FOWLER, L.E. 1979. Hatching success and nest predation in the roughly or exposed to harsh conditions, and poorly tied twine can green sea turtle, Chelonia mydas, at Tortuguero, Costa Rica. result in a nest cover falling apart. Freshly cut bamboo was found to Ecology 60: 946-955. be much sturdier and more durable than dry bamboo, and weaving FUENTES, M., C. LIMPUS & M. HAMAN. 2011. Vulnerability bamboo pieces together was more effective than tying bamboo of sea turtle nesting grounds to climate change. Global Change pieces together. If bamboo nest covers are to be used in other Biology 17: 140-153. locations, bamboo must be readily available and abundant enough for continual use. HONARVAR, S., M.C. BRODSKY, E.P. VAN DEN BERGHE, M.P. In conclusion, predation is a serious threat to sea turtle eggs in our O’CONNOR & J.R. SPOTILA. 2016. Ecology of olive ridley sea study region of Carate, Costa Rica. Dogs pose the largest predatory turtles at arribadas at Playa La Flor, Nicaragua. Herpetologica threat, and there is evidence to suggest that dogs may scare away 72: 303-308. more natural predators. Bamboo nest covers are an effective and HONARVAR, S., M.P. O’CONNOR & J.R. SPOTILA. 2008. inexpensive method of reducing predation and should be used all Density-dependent effects on hatching success of the olive ridley Marine Turtle Newsletter No. 156, 2019 - Page 36 turtle, Lepidochelys olivacea. Oecologia 157: 221-230. Environmental Management. CABI Publishing, Wallingford, ISAKSSON, D., J. WALLANDER & M. LARSSON. 2007. UK. pp. 103-126. Managing predation on ground-nesting birds: the effectiveness of NELMS, S.E., E.M. DUNCAN, A.C. BRODERICK, T.S. nest exclosures. Biological Conservation 136: 136-142. GALLOWAY, M.H. GODFREY, M. HAMANN, P.K. LINDEQUE KAPPELLE, M. 2016. Costa Rica’s ecosystems: setting the stage. & B.J. GODLEY. 2015. Plastic and marine turtles: a review and In: Kappelle, M. (Ed.). Costa Rican Ecosystems. University of call for research. ICES Journal of Marine Science 73: 165-181. Chicago Press, Chicago, USA. pp. 3-16. NIEHAUS, A.C., D.R. RUTHRAUFF & B.J. MCCAFFERY. 2004. KURZ, D.J., K.M. STRALEY & B.A. DEGREGORIO. 2012. Out- Response of predators to Western Sandpiper nest exclosures. foxing the red fox: how best to protect the nests of the endangered Waterbirds 27: 79-82. loggerhead marine turtle Caretta caretta from mammalian O’CONNOR, J.M., C.J. LIMPUS, K.M. HOFMEISTER, B.L. predation? Oryx 46: 223-228. ALLEN & S.E. BURNETT. 2017. Anti-predator meshing may LAMARRE-DEJESUS, A.S. & C.R. GRIFFIN. 2015. Habanero provide greater protection for sea turtle nests than predator pepper powder as a potential deterrent to nest predation of turtle removal. PLoS ONE 12: 1-11. nests: a response to Burke et al. Chelonian Conservation & RATNASWAMY, M.J., R.J. WARREN, M.T. KRAMER & M.D. Biology 14: 203-204. ADAM. 1997. Comparisons of lethal and nonlethal techniques to LEI, J. & D.T. BOOTH. 2017. How best to protect the nests of the reduce raccoon depredation of sea turtle nests. Journal of Wildlife endangered loggerhead turtle Caretta caretta from monitor lizard Management 61: 368-376. predation. Chelonian Conservation & Biology 16: 246-249. RUIZ-IZAGUIRRE, E., A. WOERSEM, K.C.H.A.M. EILERS, LUTCAVAGE, M.E., P. PLOTKIN, B. WITHERINGTON & P.L. S.E. WIEREN, G. BOSCH, A.J. ZIJPP & I.J.M. BOER. 2015. LUTZ. 1997. Human impacts on sea turtle survival. In: Lutz, Roaming characteristics and feeding practices of village dogs P.L. & J.A. Musick (Eds.). The Biology of Sea Turtles. Volume scavenging sea-turtle nests. Animal Conservation 18: 146-156. 1. CRC Press, Boca Raton, Florida. pp. 387-410. THAYER, G., K. BJORNDAL, J. OGDEN, S. WILLIAMS MAULANY, R.I., D.T. BOOTH & G.S. BAXTER. 2012. Emergence & J. ZIEMAN. 1984. Role of larger herbivores in seagrass success and sex ratio of natural and relocated nests of olive ridley communities. Estuaries 7: 351-376. turtles from Alas Purwo National Park, East Java, Indonesia. WAINWRIGHT, M. 2007. The Mammals of Costa Rica. A Natural Copeia 2012: 738-747. History and Field Guide. Cornell University Press, Ithaca, N.Y. MINCA, C. & M. LINDA. 2000. Ecotourism on the edge: the and London. 281pp. case of Corcovado National Park, Costa Rica. In: Font, X. & WHITING, S.D. & A.U. WHITING. 2011. Predation by the J. Tribe (Eds.). Forest Tourism and Recreation. Case Studies in saltwater crocodile (Crocodylus porosus) on sea turtle adults, eggs, and hatchlings. Chelonian Conservation and Biology 10: 198-205.

Marine Turtle Newsletter No. 156, 2019 - Page 37 Albinism In Florida Green Turtle (Chelonia mydas) Hatchlings: Ratio-Based Evidence Of Basic Mendelian Recessiveness

Justin R. Perrault1 & Christina M. Coppenrath1,2 1Loggerhead Marinelife Center, 14200 U.S. Highway One, Juno Beach, FL 33408 USA (E-mail: [email protected]); 2Florida Atlantic University, 777 Glades Road, Boca Raton, FL 33431 USA ([email protected])

On 21 July 2017, a nesting green turtle (Chelonia mydas) measuring With sea turtles, it is not uncommon to find one or two hatchlings 97.5 cm in curved carapace length laid a clutch of eggs in Juno with pigmentation anomalies from a single clutch (Pritchard 1979). Beach, Florida USA. This turtle was fitted with two inconel Finding numerous hatchlings with pigment abnormalities is much flipper tags on the forelimbs (left: EEN126, right: EEN128) and a rarer. The number of albino hatchlings produced from this nest passive integrated transponder (PIT) tag in the right front flipper nearly mirrors a nest of loggerhead (Caretta caretta) hatchlings (989001001238560). On 3 September, her clutch of 98 hatchlings from 1994 in Brazil that produced 22 albino hatchlings out of 98 emerged from the nest that was being monitored for a study on total hatchlings (Marcovaldi et al. 1995). The Brazilian loggerhead maternal transfer of cheloniid herpesvirus 5 (ChHV5). To our nest had a hatching success of 87.5% and an incubation period of surprise, 23 albino turtles made up a portion of those 98 hatchlings 52 days. The green turtle nest from our study incubated for 45 days, (Fig. 1). Upon excavation of the clutch, we observed seven with a hatching success of 85.2%, which is higher, in comparison, unhatched eggs, three of which contained albino embryos, and ten than the average hatching success of 27 other nests from the ChHV5 dead pipped eggs/hatchlings, three of which were albino; 25% of viral transfer study (mean ± SD = 66.0% ± 22.6%), suggesting that the clutch was phenotypically albino: albinism, in this case did not impact developmental success. In birds and snakes, albinism is an autosomal recessive trait 23 live albinos + 3 dead albino embryos + 2 dead pipped albinos (Sage 1962; Bechtel & Bechtel 1989) that when inherited results in = 98 hatched eggs + 7 unhatched eggs + 10 dead pipped eggs enzymatic deficiencies of melanin metabolism during development (Erickson & Kaefer 2015). A similar genetic pattern has been 29 albinos = 25.2% 115 total eggs Figure 1. (a) Albino hatchlings from the same clutch; two normally pigmented hatchlings were included for comparison. Extra vertebral and lateral scutes (i.e., scute abnormalities) are indicated by the black arrowheads. Photo credit: Bethany Augliere. (b) Albino hatchling green turtle. The red eyes indicate a lack of ocular melanin pigment, allowing capillary blood to be seen through the retina. Photo credit: Bethany Augliere. (c) For comparison, a leucistic hatchling green turtle from a separate clutch from 2017. This individual was the only abnormally pigmented hatchling in its clutch. Leucistic animals lack melanin and may lack other pigments in the skin, but have pigmented eyes. Photo credit: Christina Coppenrath. a

b c Marine Turtle Newsletter No. 156, 2019 - Page 38 PMother pMother abnormal retinal pathways to the brain (Sage 1962; Guillery 1986; Godrey & Mrosovsky 1995). However, an amelanistic loggerhead PFpM (25%): PFPM (25%): was observed nesting in Queensland, Australia in 1977 & 1978 PFather normal pigment, normal pigment (Limpus et al. 1979). We were unable to test the seafinding behavior albinism carrier of the hatchlings documented here due to lack of permits and the pFPM (25%): impending Hurricane Irma; however, this will be studied in any pFpM (25%): pFather normal pigment, future encounters with albino hatchlings. albinism albinism carrier For follow up studies, blood and morphometric measurements were collected from every hatchling from this nest in an effort to Figure 2. Hypothetical single trait Punnett square representing determine paternity, health and morphological differences between a possible scenario from this clutch of green turtle eggs. hatchlings with and without albinism, and the gene responsible for Based on the 3:1 ratio of normally pigmented hatchlings to this disorder. Those results will be published as part of a larger albino hatchlings, this clutch most likely had a single father. study on the health impacts of albinism in green turtle hatchlings. “P” and “p” represent the dominant and recessive alleles for presence and absence of pigment, respectively. BECHTEL, H.B. & E. BECHTEL. 1989. Color mutations in the corn snake (Elaphe guttata guttata): review and additional breeding predicted in sea turtles (Godfrey & Mrosovsky 1995); however, data. Journal of Heredity 80: 272-276. this has not been confirmed. Recently, corn snakes (Pantherophis BUSTARD, H.R. & C. LIMPUS. 1969. Observations on the flatback gutattus) were used as model species to investigate the mutation turtle Chelonia depressa Garman. Herpetologica 25: 29-34. resulting in amelanism in reptiles. This study revealed that mutation CLAY, M. 1935. The occurrence of albinos in a brood of the common of the OCA2 gene is responsible for the pigment disorder (Saenko water snake, Natrix sipedon (L.). Copeia 1935: 115-118. et al. 2015). Based on the ratio of albino hatchlings to total eggs in ERICKSON, J. & I.L. KAEFER. 2015. Multiple leucism in a nest the green turtle clutch from this study, it is likely that albinism in sea of the yellow-spotted Amazon River turtle, Podocnemis unifilis. turtles is a result of basic Mendelian recessiveness as indicated by a Salamandra 51: 273-276. Punnett square for a single trait (Fig. 2), with 25% of the offspring FLETEMEYER, J. 1977. Rare albino turtle. Sea Frontiers 23: 233. carrying both autosomal recessive copies of the allele leading to the phenotypic expression of the lack of pigment. Additionally, based FOWLER, L.E. 1979. Hatching success and nest predation in the on the near perfect ratio of 3:1 for normally pigmented to albino green sea turtle, Chelonia mydas, at Tortuguero, Costa Rica. hatchlings, it is likely that only one father contributed to this clutch Ecology 60: 946-955. (despite known occurrences of multiple paternity in green turtles: GODFREY, M.H. & N. MROSOVSKY. 1995. Comment on albino Ireland et al. 2003). Perhaps the mother and father were related, as sea turtle hatchlings in Brazil. Marine Turtle Newsletter 69: 10-11. both would have to be carriers of this rare allele. Our interpretation is GUILLERY, R.W. 1986. Neural abnormalities of albinos. Trends hypothetical at this time and support or lack of support will depend in Neurosciences 9: 364-367. upon genetic analyses. It also has been suggested that environmental HEWAVISENTHI, S. 1990. Abnormal hatchlings of green and olive influences including stress and habitat quality can impact the ridley turtles, Victor Hasselblad Hatchery, Sri Lanka. Marine occurrence of this disorder (McCardle 2012). Turtle Newsletter 50: 15-16. Albinism has been observed in all vertebrate groups (cyclostomes: HITCHINS, P.M. & & O. BOURQUIN. 2005: Partial albinism in Jensen 1959; elasmobranchs: Sandoval-CaStillo et al. 2006; the hawksbill turtle (Eretmochelys imbricata) on Cousine Island, osteichthyes: Manoel et al. 2017; amphibians: López & Ghirardi Seychelles. Phelsuma 14: 103-104. 2011; reptiles: Clay 1935; Bechtel & Bechtel 1981; Kar & Bustard IRELAND, J.S., A.C. BRODERICK, F. GLEN, B.J. GODLEY, 1982; Spadola & Di Toro 2007; birds: Sage 1962; mammals: Uieda G.C. HAYS, P.L.M. LEE & D.O.F. SKIBINSKI. 2003. Multiple 2000), including all seven sea turtle species (Bustard & Limpus paternity assessed using microsatellite markers, in green turtles 1969; Whitmore & Dutton 1985; Hewavisenthi 1990; Godfrey Chelonia mydas (Linnaeus, 1758) of Ascension Island, South & Mrosovsky 1995; Marcovaldi et al. 1995; Johnson et al. 1999; Atlantic. Journal of Experimental Marine Biology and Ecology Türkozan & Durmuş 2001; Hitchins & Bourquin 2005; Sönmez 291: 149-160. & Özdilek 2011). Generally, albinism in marine turtles is rare, JENSEN, D. 1959. Albinism in the California hagfish Eptatretus with less than 1% of embryos/hatchlings expressing this condition stoutii. Science 130: 798. (Fowler 1979; Kaska & Downie 1999; Hitchins & Bourquin, 2005). JOHNSON, S.A., A.L. BASS, B. LIBERT, M. MARSHALL & D. Observations of albinism in larger life stages are extremely rare FULK. 1999. Kemp’s ridley (Lepidochelys kempii) nesting in (Fletemeyer 1977; Sönmez & Özdilek 2011), which indicates little Florida. Florida Scientist 62: 194-204. to no chance of survival in sea turtles with abnormal pigmentation. KAR, S.K. & H.R. Bustard. 1982. Occurrence of partial albinism in Understandably, this trait is not selected for in the wild as albino a wild population of the saltwater crocodile (Crocodylus porosus, sea turtles likely suffer higher mortality rates due to the inability Schneider) in Orissa, India. British Journal of Herpetology 6: to camouflage (Erickson & Kaefer 2015), as well as anatomical 220-221. abnormalities (e.g., cleft palate, scute anomalies; Kaska & Downie KASKA, Y. & J.R. Downie. 1999. Embryological development of 1999, Turkozan & Durmus 2001; Hitchins & Bourquin, 2005; sea turtle (Chelonia mydas, Caretta caretta) in the Mediterranean. Sönmez & Özdilek 2011; Fig. 1), disease susceptibility (Hayley- Zoology in the Middle East 19: 55-69. McCardle 2012), and potential effects on seafinding behavior due to LIMPUS, C.J., K. MILLER & E. MCLACHLAN. 1979. A record Marine Turtle Newsletter No. 156, 2019 - Page 39 of a breeding amelanic loggerhead turtle. Herpetological Review SAGE, B.L. 1962. Albinism and melanism in birds. British Birds 10: 6. 55: 201-225. LÓPEZ, J.A. & R. GHIRARDI. 2011. First record of albinism in SANDOVAL-CASTILLO, J., E. MARIANO-MELENDEZ & C. Rhinella fernandezae (Gallardo 1957). Belgian Journal of Zoology VILLAVICENCIO-GARAYZAR. 2006. New records of albinism 141: 59-61. in two elasmobranchs: the tiger shark Galeocerdo cuvier and the MANOEL, P.S., E.R. ONO & M.I.B. ALVES. 2017. First report giant electric ray Narcine entemedor. Cybium 30: 191-192. of albinism in the South American catfish Imparfinis mirini SÖNMEZ, B. & S.Y. ÖZDILEK. 2011. Morphologic characters of (Siluriformes: Heptapteridae). Revista Mexicana de Bioversidad albino green turtle (Chelonia mydas) hatchlings on Samandag 88: 471-473. beach in Turkey. Marine Turtle Newsletter 131: 46-47. MARCOVALDI, M.Â., E.P. LIMA, & R. PENTEADO. 1995. SPADOLA, F. & F. DI TORO. 2007. Complete albinism in a Albino sea turtles hatchlings in Brazil. Marine Turtle Newsletter Podarcis muralis newborn. Acta Herpetologica 2: 49-51. 69: 10. MCCARDLE, H. 2012. Albinism in wild vertebrates. M.Sc. thesis. TÜRKOZAN, O. & S.H. DURMUŞ. 2001. Albino loggerhead and Texas State University-San Marcos, San Marcos, Texas, USA. green turtle (Caretta caretta and Chelonia mydas) hatchlings in 71 pp. Turkey. Zoology in the Middle East 24: 133-136. PRITCHARD, P.C.H. 1979. Encyclopedia of Turtles. T.F.H. UIEDA, W. 2000. A review of complete albinism in bats with five Publications, Inc. Ltd., Neptune, New Jersey. 895 pp. new cases from Brazil. Acta Chiropterologica 2: 97-105. SAENKO, S.V., S. LAMICHHANEY, A.M. BARRIO, N. RAFATI, WHITMORE, C.P. & P.H. DUTTON. 1985. Infertility, embryonic L. ANDERSSON & M.C. MILINKOVITCH. 2015. Amelanism mortality and nest-site selection in leatherback and green sea in the corn snake is associated with the insertion of an LTR- turtles in Suriname. Biological Conservation 34: 251-272. retrotransposon in the OCA2 gene. Scientific Reports 5: 17118.

Marine Turtle Newsletter No. 156, 2019 - Page 40 Marine Debris and Marine Turtles in the Venezuelan Guajira Peninsula: A New Menace

Héctor Barrios-Garrido1,2,3,4, María José Petit-Rodríguez1,2, Nínive Espinoza-Rodríguez1 & Natalie Wildermann1,2,3,4 1Grupo de Trabajo en Tortugas Marinas del Golfo de Venezuela GTTM-GV, Venezuela (E-mail: [email protected]); 2Laboratorio de Ecología General; Centro de Modelado Científico - CMC, La Universidad del Zulia (LUZ) Maracaibo 4001, Zulia, Venezuela (E-mail: [email protected]); 3TropWATER - Centre for Tropical Water & Aquatic Ecosystem Research, James Cook University, Australia (E-mail: [email protected]); 4Marine Turtle Research, Ecology and Conservation Group, Department of Earth, Ocean and Atmospheric Science, Florida State University, Tallahassee 32306, FL, USA (E-mail: [email protected])

Marine megafauna is impacted by human-generated waste (Grant debris on marine turtle populations along the Venezuelan Guajira et al. 2012). Recent evaluations highlight the major threat posed Peninsula on the GV. by plastic pollution on the survival of charismatic megafauna, The Venezuelan Guajira Peninsula is located in the Zulia state, including penguins, aquatic mammals, seabirds, and marine turtles in north-western Venezuela, and forms the western side of the Gulf (González Carman et al. 2014; Wedemeyer-Strombel et al. 2015; of Venezuela (Fig. 1). It is considered an important feeding area for Pham et al. 2017). Indeed, marine debris appears to affect all marine at least four different species of marine turtles (Barrios-Garrido turtle species in all the habitats they use during their complex life et al. 2017b). Although its human population is low in numbers cycle, including migratory routes, seasonal feeding grounds, and (Almanza Vides et al. 2017), the Venezuelan Guajira Peninsula is overwintering areas (Duncan et al. 2017, In press). highly affected by marine pollution (Pulido Petit et al. 2017). It The Gulf of Venezuela (GV), located in the southern Caribbean, occurs mainly due to constant blowing effect of the trade winds and is considered to be one of the most important feeding grounds for sea currents along the coastal area (Morán et al. 2014; Gutierrez marine turtles in the country (Buitrago et al. 2008; Guada & Sole Leones et al. 2015). 2000). However, marine turtles found in the GV are exposed to As part of regular scientific patrols (in-water and artisanal port several anthropogenic threats, primarily: (a) take of immature surveys) carried out by members of the NGO “Grupo de Trabajo en and adult-sized individuals of at least four species; (b) trade of Tortugas Marinas del Golfo de Venezuela (GTTM-GV)” (Barrios- marine turtle parts or products; (c) habitat degradation due to Garrido & Montiel-Villalobos 2016), 55 stranded marine turtles coastal development, particularly through dredging operations for (Chelonia mydas, Eretmochelys imbricata, Dermochelys coriacea, navigation channel management in the southern portion of the GV; and Caretta caretta) were found in the study area between January (d) exposure to frequent oil spills (Barrios-Garrido 2018). Moreover, and December 2011. In addition, in June 2016, during a separate recent studies have revealed an increase in exposure to some threats survey, we rescued a juvenile green turtle on Zapara Island with such as contamination (Barrios-Garrido et al. 2013; Petit-Rodriguez evidence of plastic ingestion. et al. 2013). Here we present further evidence of the threat of marine In all cases, we collected standardized data from the stranded turtles, including curved carapace length (CCL), and we attempted to determine the cause of stranding. Necropsies were carried out when we encountered dead turtles. Due to logistic challenges in transporting carcasses to Maracaibo city (the state capital), only six turtles were necropsied in the Laboratory of General Ecology, at the University of Zulia; the others were necropsied in the field. From the 55 necropsied turtles, we identified marine debris in three cases (5%) of all 2011 samples. However, in only one turtle was marine debris identified as the cause of death. Note that the three turtles identified with marine debris were from the group of six carcasses necropsied under optimal conditions in the Laboratory of General Ecology in Maracaibo. Herein, we detailed the three records from 2011: (a). Plastic ingestion (two green turtles). Ingested plastic materials were collected during post mortem digestive tracts of two turtles with CCL measurements of 29.1 cm and 32.2 cm. One turtle originally stranded in Kazuzain (Middle Guajira; Fig. 1) and the second turtle was found alive in Zapara Island (Low Guajira; Fig.1) but subsequently passed away during rehabilitation. During both necropsies, the stomach and intestinal contents were rinsed and Figure 1. Study area. Gulf of Venezuela. Kazuzain locality sieved in order to identify any plastic. We identified 8 plastic items is marked with circle (●) , and Zapara Island is marked with in the two stranded turtles: (I) polyethylene (low and high density) a a square (■). Marine Turtle Newsletter No. 156, 2019 - Page 41 plastic bags; (II) polyamide (nylon); and (III) polyvinyl chloride (Ministerio del Poder Popular para el Ambiente, now Ecosocialism (PVC). and Water Ministry) via scientific licenses 828, 886, and 1224. (b). Entanglement record (one green turtle). During an in-water ALMANZA VIDES, K., R. ALMANZA VIDES & S. PIMIENTA fieldtrip in Kazuzain (Middle Guajira; Fig. 1), we found a dead GÓMEZ. 2017. Reflexiones sobre la Cosmovision y Cosmogonia entangled juvenile turtle in a 15 m long monofilament net (10 de la etnia Wayuu: Relevancia para la practica educativa. cm stretch mesh size). The turtle was in a state of advanced REDHECS 23: 198-217. decomposition and its CCL = 52.1 cm. BARRIOS-GARRIDO, H. 2018. Socio-economic drivers affecting One record from June-2016: marine turtle conservation status: causes and consequences. (c). Plastic intake (one green turtle). During a survey in Zapara PhD Thesis, College of Science and Engineering, James Cook Island (Low Guajira; Fig. 1), we rescued a juvenile green turtle (CCL University. Townsville, Australia. 287 pp. = 27.4 cm). Following our standard protocols, we took the turtle to a rehabilitation facility in Maracaibo. We subsequently found traces BARRIOS-GARRIDO, H., J. BOLIVAR, L. BENAVIDES, of plastic in its faeces. We collected 11 items, which we identified J. VILORIA, F.N. DUGARTE-CONTRERAS & N. as rigid and soft plastic bag pieces of low-density polyethylene WILDERMANN. 2017a. Evaluación de la pesquería de palangre (LDPE), polypropylene (dry goods), and clear cellophane from artesanal y su efecto en la Raya Hocicona (Dasyatis guttata) cellulose (cookie wrappers and confectionery bags). Due to the en Isla Zapara-Golfo de Venezuela. Latin American Journal of nature and size of the items collected, we were unable to weigh the Aquatic Research 45: 302-310. plastic items. After two weeks, no more plastic items were identified BARRIOS-GARRIDO, H., N. ESPINOZA-RODRÍGUEZ, D. from the turtle’s faeces, and the animal was cleared for release in ROJAS-CAÑIZALES, J. PALMAR, N. WILDERMANN, M. the same locality where it was rescued. MONTIEL-VILLALOBOS & M. HAMANN. 2017b. Trade Although relatively infrequent, we show that marine debris of marine turtles along the southwestern coast of the Gulf of poses a threat to sea turtles in the Gulf of Venezuela. Although Venezuela. Marine Biodiversity Records 10: 1-12. our survey was not designed specifically to check for presence of BARRIOS-GARRIDO, H. & M.G. MONTIEL-VILLALOBOS. plastics in sea turtles, the fact that we found some suggests that the 2016. Strandings of Leatherback turtles (Dermochelys coriacea) problem warrants detailed scrutiny. We recognized the high cost for along the western and southern coast of the Gulf of Venezuela. standardized patrols for stranded turtles under the current economic Herpetological Conservation and Biology 11: 244-252. situation of Venezuela, especially in the Zulia state. However, at a BARRIOS-GARRIDO, H., M.J. PETIT-RODRIGUEZ, E. minimum future research projects and management plans should MORENO & N. WILDERMANN. 2013. Ghost nets: a new include the evaluation of marine debris impacts to sea turtles as a hazard to sea turtles in the Gulf of Venezuela. In: Tucker T., L. priority action (Rees et al. 2016; Barrios-Garrido 2018). Belskis L, A. Panagopoulou, A. Rees M. Frick, K. Williams, R. The low observed incidence of entanglement in nets is likely LeRoux & K. Stewart (Comps). Proceedings of the 33rd Annual to be related to the high costs of the fishing nets for the local Symposium on Sea Turtle Biology and Conservation. NOAA Tech fishermen in this area (Wayuú indigenous communities), who tend Memo NMFS-SEFSC-645. p 89. to reuse their fishing nets, and thereby rarely discard any fishing gear. Furthermore, based on the characteristics of the net with BUITRAGO, J., H.J. GUADA & E. DOYLE. 2008. Conservation the entangled turtle, it likely came from one of the bigger fishing science in developing countries: an inside perspective on the ships (locally called ‘Bongos’), which come from the southern struggles in sea turtle research and conservation in Venezuela. communities Gulf of Venezuela, a non-indigenous territory (Casas Environmental Science and Policy 11: 562-578. & Hernandez 2010; Barrios-Garrido et al. 2017a). CARON, A.G.M., C.R. THOMAS, K.L.E. BERRY, C.A. MOTTI, Overall, it is necessary to develop systematic assessments in E. ARIEL & J.E. BRODIE. 2018. Ingestion of microplastic debris order to evaluate the impact of marine debris (plastic pollution, by green sea turtles (Chelonia mydas) in the Great Barrier Reef: ghost nets, among others) in the study area (Guada & Sole 2000). Validation of a sequential extraction protocol. Marine Pollution We recognise that marine debris may be impacting marine turtles in Bulletin 127: 743-751. other ways that we have yet to observe (Duncan et al. 2017; Caron CASAS, C. & J. HERNANDEZ. 2010. La region noroccidental et al. 2018; Vélez-Rubio et al. 2018). We suggest that it would be de Venezuela como area de criadero de tiburones de las familias highly beneficial to involve all fishing communities connected by Carcharhinidae y Sphyrnidae In: FEC-LUZ, XII Jornadas the waters of the Gulf of Venezuela in the monitoring of marine Nacionales de Investigacion y Postgrado. Facultad Experimental debris and its impacts to marine turtles, and to evaluate all potential de Ciencias, La Universidad del Zulia, Maracaibo, Venezuela. p biological, environmental and social consequences of this threat. 110. Acknowledgements. We are thankful to members of the fisher DUNCAN, E.M., Z.L.R. BOTTERELL, A.C. BRODERICK, T.S. communities from Kazuzain, Zapara Island, for participating in GALLOWAY, P.K. LINDEQUE, A. NUNO & B.J. GODLEY. the RAO-Zulia network. We also appreciate the support of MTN’s 2017. A global review of marine turtle entanglement in editorial team and anonymous reviewers for their help improving anthropogenic debris: a baseline for further action. Endangered our manuscript. We express our gratitude to the vast group of Species Research 34: 431-448. volunteers from the ‘Grupo de Trabajo en Tortugas Marinas del DUNCAN, E.M., A.C. BRODERICK, W.J. FULLER, T.S. Golfo de Venezuela: GTTM-GV’ and the University of Zulia who GALLOWAY, M.H. GODFREY, M. HAMANN, C.J. LIMPUS, participated and supported our surveys in the study area. This P.K. LINDEQUE, A.G. MAYES, L.C.M. OMEYER, D. research was authorised by Venezuela´s Environmental Ministry Marine Turtle Newsletter No. 156, 2019 - Page 42 SANTILLO, R.T.E. SNAPE & B.J. GODLEY. In press. NMFS-SEFSC-645. p 111. Microplastic ingestion ubiquitous in marine turtles. Global PHAM, C.K., Y. RODRÍGUEZ, A. DAUPHIN, R. CARRIÇO, Change Biology. J.P.G.L. FRIAS, F. VANDEPERRE, V. OTERO, M.R. SANTOS, GONZÁLEZ CARMAN, V., E.M. ACHA, S.M. MAXWELL, D. H.R. MARTINS, A.B. BOLTEN & K.A. BJORNDAL. 2017. ALBAREDA, C. CAMPAGNA & H. MIANZAN. 2014. Young Plastic ingestion in oceanic-stage loggerhead sea turtles (Caretta green turtles, Chelonia mydas, exposed to plastic in a frontal area caretta) off the North Atlantic subtropical gyre. Marine Pollution of the SW Atlantic. Marine Pollution Bulletin 78: 56-62. Bulletin 121: 222-229. GRANT, S.B., J.-D. SAPHORES, D.L. FELDMAN, A.J. PULIDO PETIT, G., N. WILDERMANN & H. BARRIOS- HAMILTON, T.D. FLETCHER, P.L.M. COOK, M. GARRIDO. 2017. Comunidades de macroinvertebrados asociadas STEWARDSON, B.F. SANDERS, L.A. LEVIN, R.F. AMBROSE, a piscinas de marea del litoral rocoso Punta Perret, estado Zulia, A. DELETIC, R. BROWN, S.C. JIANG, D. ROSSO, W.J. Venezuela. Ciencia 25: 15-28. COOPER & I. MARUSIC. 2012. Taking the “waste” out REES, A.F., J. ALFARO-SHIGUETO, P.C.R. BARATA, K.A. of “wastewater” for human water security and ecosystem BJORNDAL, A.B. BOLTEN, J. BOURJEA, A.C. BRODERICK, sustainability. Science 337: 681. L.M. CAMPBELL, L. CARDONA, C. CARRERAS, P. CASALE, GUADA, H. & G. SOLE. 2000. WIDECAST Plan de Acción para la S.A. CERIANI, P.H. DUTTON, T. EGUCHI, A. FORMIA, Recuperación de las Tortugas Marinas de Venezuela. In: A. Suarez M.M.P.B. FUENTES, W.J. FULLER, M. GIRONDOT, M.H. (Ed.). Informe Técnico del PAC UNEP Caribbean Environment GODFREY, M. HAMANN, K.M. HART, G.C. HAYS, S. Programme, Kingston, Jamaica. pp. 112+xiv. HOCHSCHEID, Y. KASKA, M.P. JENSEN, J.C. MANGEL, GUTIERREZ LEONES, G.A., M.A. CORREA RAMIREZ & J.A. MORTIMER, E. NARO-MACIEL, C.K.Y. NG, W.J. S.E. HORMAZABAL FRITS. 2015. Análisis de la variabilidad NICHOLS, A.D. PHILLOTT, R.D. REINA, O. REVUELTA, espacio-temporal del sistema de surgencia de La Guajira en el G. SCHOFIELD, J.A. SEMINOFF, K. SHANKER, J. TOMAS, dominio espacio-frecuencia, empleando el MTM-SVD (Multi J.P. VAN DE MERWE, K.S. VAN HOUTAN, H.B. VANDER Taper Method Singular Value Decomposition). Boletín Científico ZANDEN, B.P. WALLACE, K.R. WEDEMEYER-STROMBEL, CIOH 33: 87-106. T.M. WORK & B.J. GODLEY. 2016. Are we working towards global research priorities for management and conservation of sea MORÁN, L., H. SEVEREYN & H. BARRIOS-GARRIDO. 2014. turtles? Endangered Species Research 31: 337-382. Moluscos bivalvos perforadores de rocas coralinas submareales de la alta Guajira, Golfo de Venezuela. Interciencia 39: 136-139. VÉLEZ-RUBIO, G.M., N. TERYDA, P.E. ASAROFF, A. ESTRADES, D. RODRIGUEZ & J. TOMÁS. 2018. Differential PETIT-RODRIGUEZ, M.J., N. WILDERMANN, F. VERA, A. impact of marine debris ingestion during ontogenetic dietary shift PINEDA & H. BARRIOS-GARRIDO. 2013. First report of plastic of green turtles in Uruguayan waters. Marine Pollution Bulletin items in stomach and intestinal contents of green turtles (Chelonia 127: 603-611. mydas) in the Gulf of Venezuela. In: Tucker T., L. Belskis, A. Panagopoulou, A. Rees, M. Frick, K. Williams, R. LeRoux & K. WEDEMEYER-STROMBEL, K.R., G.H. BALAZS, J.B. Stewart (Comps.). Proceedings of the 33rd Annual Symposium JOHNSON, T.D. PETERSON, M.K. WICKSTEN & P.T. on Sea Turtle Biology and Conservation. NOAA Tech Memo PLOTKIN. 2015. High frequency of occurrence of anthropogenic debris ingestion by sea turtles in the North Pacific Ocean. Marine Biology 162: 2079-2091.

Marine Turtle Newsletter No. 156, 2019 - Page 43 REPORTS Report: The Second Annual Workshop on the Use of UAVs in Sea Turtle Research and Conservation at the 38th International Sea Turtle Symposium: 19 Feb 2018

ALan F. Rees1 & Raymond R. Carthy2 1Centre for Ecology and Conservation, University of Exeter, Penryn, Cornwall, TR10 9FE UK (E-mail: [email protected]); 2U.S. Geological Survey, Florida Cooperative Fish & Wildlife Research Unit, PO Box 110485, Gainesville, FL 32611-0430 USA (E-mail: [email protected])

The second ‘drone workshop’ was held in Kobe, Japan and was BEVAN, E., T. WIBBELS, E. NAVARRO, M. ROSAS, B.M.Z attended by around 50 participants in a room for 30 people with NAJERA, L. SARTI, F. ILLESCAS, J. MONTANO, L.J. PEÑA seating for even fewer (Fig. 1)! The workshop was designed to & P. BURCHFIELD. 2016. Using unmanned aerial vehicle (UAV) follow on from the previous year’s inaugural gathering held at the technology for locating, identifying, and monitoring courtship 37th International Sea Turtle Symposium in Las Vegas (Rees et al. and mating behavior in the green turtle (Chelonia mydas). 2017). It was divided into two sections. The first covered the basics Herpetological Review 47: 27-32. of drone technologies and considerations when designing a project REES, A.F., M.R. VARELA & B.J. GODLEY. 2017. The use and the second expanded more on the methods and findings of of unmanned aerial vehicles (UAVs) in sea turtle research: a ‘real-life’ research and recent published studies. workshop report. Marine Turtle Newsletter 154: 20-21. AFR opened the workshop with an overview of drone styles REES, A.F., L. AVENS, K. BALLORAIN, E. BEVAN, A.C. and capabilities, listing the most popular brands and capabilities of BRODERICK, R.R. CARTHY, M.J.A. CHRISTIANEN, G. drones used in sea turtle research. He then explained the types of DUCLOS, M.R. HEITHAUS, D.W. JOHNSTON, J.C. MANGEL, data capture and use and ended with a recap of a review paper on F. PALDINO, K. PENDOLY, R.D. REINA, N.J. ROBINSON, R. drones and sea turtle research and conservation that was published RYAN, S.T. SYKORA-BODEY, D. TILLEY, M.R. VARELA, the following day (Rees et al. 2018). The second half of the opening E.R. WHITMAN, P.A. WHITTOCK & T. WIBBELS. 2018. The section comprised a presentation by RRC covering “Preparation, potential of unmanned aerial systems for sea turtle research and Precautions and Pitfalls” in drone-related scientific data collection. conservation: a review and future directions. Endangered Species Section two kicked off with a presentation from Paul Whittock Research 35:81-100. of Pendoley Environmental describing two case studies on nesting beach monitoring and topographic modeling undertaken by the SCHOFIELD, G., K. PAPAFITSOROS, R. HAUGHEY & K. company. This was followed by a presentation by Vanessa Bezy who KATSELIDIS. 2017a. Aerial and underwater surveys reveal provided updates and insights on her work monitoring olive ridley temporal variation in cleaning-station use by sea turtles at arribadas in Costa Rica, building on her recently published methods a temperate breeding area. Marine Ecology Progress Series paper (Sykora-Bodey et al. 2017). RRC then reviewed UAS projects 575:153-164. and platforms of the University of Florida Unmanned Aircraft SCHOFIELD, G., K.A. KATSELIDIS, M.K.S. LILLEY, R.D. Systems Research Program that began in 1999, and showed some REINA & G.C. HAYS. 2017b. Detecting elusive aspects of Kemp’s ridley arribada survey imagery provided by Thane Wibbels. wildlife ecology using drones: new insights on the mating The section concluded with AFR briefly appraising three further dynamics and operational sex ratios of sea turtles. Functional published articles that used drones as tools in sea turtle research Ecology 31:2310-2319. in nearshore waters (Bevan et al. 2016, Schofieldet al. 2017a,b). SYKORA-BODIE, S.T., V. BEZY, D.W. JOHNSTON, E. NEWTON These presentations were followed by open discussion that & K.J. LOHMANN. 2017. Quantifying nearshore sea turtle included further potential uses for drones in surveillance operations densities: applications of unmanned aerial systems for population and the use of assemble-it-yourself fixed-wing drones as cheaper assessments. Scientific Reports 7:17690. alternatives to commercially available ready-to-fly models.

Figure 1. Dedicated attendees of the 2nd annual ‘drone workshop’. The lucky ones got seats but there was enough wall and floor space for everyone. Marine Turtle Newsletter No. 156, 2019 - Page 44 President’s Report, 38th Annual Symposium on Sea Turtle Biology & Conservation, Kobe, Japan, 18-23 February 2018

Yoshimasa Matsuzawa President, International Sea Turtle Society; Sea Turtle Association of Japan, Hirakata, Japan (E-mail: [email protected])

The 38th International Sea Turtle Symposium was held in Kobe, Long-term Success of Sea Turtle Conservation Projects; and The Art Hyogo, Japan from 18 to 23 February, 2018. The theme of the of Writing Science lead by the Student Committee. Seven regional Symposium was “Beyond Protection of Sea Turtles.” As a result of meetings were held allowing participants from over 54 countries decades of hard work, we have witnessed the protection and recovery around the world to discuss specific problems that impact their of some sea turtle populations while at the same time facing a myriad regions. These were: Africa, East Asia, Indian Ocean and South- of threats and issues to others. As researchers and conservationists, east Asia (IOSEA), Mediterranean, Pacific Islands/Oceania; Latin it is easy to get so caught up in the day-to-day activities of our work, America (RETOMALA), and the 28th Annual Japanese Sea Turtle and we lose sight of our mission and goals. It is important to step Symposium. Besides these workshops and regional meetings, the back, envision our goals and discuss them with colleagues, and take IUCN Marine Turtle Specialist Group (MTSG) was also held as a our efforts “beyond protection.” side meeting in the Tuesday evening. The Kobe Municipal Suma Aqualife Park and the Sea Turtle Main Symposium Program. Opening Remarks from the ISTS Association of Japan (STJ) were key partners in hosting the President Yoshimasa Matsuzawa inaugurated the main symposium Symposium, providing personnel and access to their facilities. program. A Japanese traditional Shinto ritual to pray for safety A total of 632 people registered for the Symposium, all of who and success of the symposium followed his words. This special came together to learn about sea turtles and conservation of ocean ceremony was conducted by Mr. Miyajima, who is a chief priest of resources. The main venue for the symposium was the Kobe “Urashima shrine,” the enshrined deity of which is Urashimako – a Convention Center, Kobe, Japan. In addition to oral and poster model of Urashima Taro who is drawn in the logo of the symposium. presentations, the symposium program included 10 workshops, During the Shinto ritual, he invited the deity and recited a Shinto seven regional meetings, the annual Marine Turtle Specialist Group prayer called Norito that praises virtues of the deity and prays for meeting, three special sessions, as well as several fun and productive benefits and protection. While enjoying the beauty of traditional social networking events, which were held at Ariston Hotel, Portopia prayer, participants spent a bit of time thinking of the relationship Hotel, and Suma Aqualife Park. Overall the meeting was exciting between sea turtles and ancient people and prayed for the success and a success from every perspective; details are offered below. of the symposium. Just after the ceremony, Dr. Naoki Kamezaki, Logo. Urashima Taro is the protagonist of this year’s Symposium from Okayama University of Science, addressed attendees with the and is featured on the meeting’s logo, representing both Japanese presentation “Historical review of relationship between sea turtle and culture and demonstrating this nation’s appreciation of sea turtles. humans in Japan: Recognition of the importance of local research Urashima Taro is a Japanese fairy tale where a fisherman rescues and management coordination.” a turtle and is rewarded with a visit to a palace under the sea. The Symposium program of oral and posters presentations ran Everyone has a version of Urashima Taro inside of them, urging from Tuesday, 20 February through Friday, 23 February. The Oral them to protect, understand and discover the mysteries of the sea and Poster presentations consisted of traditional session categories, turtles, with no personal expectations other than the intrinsic joy of including Anatomy, Physiology and Health; In-Water Biology; knowing that sea turtles and their habitats are protected. The logo Nesting Biology; Population Biology and Monitoring; Fisheries was created by Moe Wajiki. and Threats; Conservation, Management and Policy; Education, Workshops and Regional Meetings. The structure of the Outreach and Advocacy; and Social, Economic and Cultural Studies. symposium in Kobe was similar to that of year’s past: 10 workshops Program Chairs Takahashi Ishihara, Tomomi Saito, Isao Kawazu and and seven regional meetings were scheduled during the two days Kei Okamoto, along with 36 Session Chairs developed an amazing prior to the symposium’s main four days of presentations, providing symposium program consisting of 139 oral papers and 199 posters the opportunity to exchange and share ideas and information presented within the sessions mentioned above. Poster presenters regarding environmental and sea turtle conservation issues, as had also the opportunity to give more details on their presentations well as cutting-edge research techniques. These meetings were as well as answering some questions during “Meet the Authors” successful and also helped bring attendees early to the symposium. scheduled after the last session of every day. The theme of the workshops were: Captive Rearing for Research In addition to these regular sessions, three special sessions were and Conservation; Geographic Information System; Introductory held. “Beyond Protection of Sea Turtle” was aimed to broaden R and Statistics; Temperature-dependent Sex Determination: the discussion on the main theme of this symposium. This session Beyond Protection of Sea Turtles; Marine Debris and Sea Turtles; consisted of short panelist presentations and discussion facilitated Western Pacific Leatherback Turtle Working Group; Sea Turtle by Kartik Shanker. Panelists were: Yoshimasa Matsuzawa, Jack Medicine and Rehabilitation; Use of Unmanned Aerial Vehicles or Frazier, Paolo Casale, Matthew Godfrey, Colin Limpus, Neca Drones in Sea Turtle Conservation and Research; Building Income Marcovaldi and Hiroyuki Suganuma (Fig. 1). Special Session “North Generating Activities Adapted to the Local Context to Ensure the Pacific Loggerhead Turtle” focused on this dynamic migratory Marine Turtle Newsletter No. 156, 2019 - Page 45 population, with experts providing an overview of each life history as well as the demonstration of a Turtle Releasing Device from a stage and highlighting the need and ongoing efforts for international model underwater pound net set up in the main tank. As participating cooperation. Line up of the experts was Jeff Seminoff, Cali Tuner co-hosts, the aquarium staff was on hand to answer questions and Tomaszewicz, Takashi Ishihara, Hideo Hatase, and Alexis Gutierrez. assist meeting attendees throughout the week. Another highlight The third Special Session was “Linking Space Exploration and of social events in Kobe was “Japan Night,” which was held Sea Turtle” where it reviewed the current conservation activities at Wednesday evening. This activity aimed to introduce a part of nesting beaches adjacent to satellite launch stations and discussed Japanese culture to attendees. People enjoyed watching performance the prospects of the space exploration and nature conservation of Japanese drum and art of calligraphy (Fig. 1), trying Kimono, with a focus on how the space industry benefits sea turtles and sea origami, Japanese wrapping cloth, and rice-cake making, as well turtle people. Jane Provancha, Mark Hamann, Sophi Baudel and as tasting rice-cake and Kobe beef. As it is typical, the Silent (from George Balazs gave presentations. During the main oral presentation the beginning of the symposium until February 22nd) and Live sessions, simultaneous English-Japanese translation was available. Auctions (on the 22 February from 7:00 -11:00 pm) were among Kobe Declaration. On the basis of a meaningful discussion at the most popular events. The auction teams successfully maximized the special session, ISTS President Yoshimasa Matsuzawa read fun and funding under new auction guidelines. The events jointly through the following personal statement at the business meeting: raised approximately US$17,000 to help students to attend future The Kobe Declaration: Beyond Protection of Sea Turtles* symposia via travel grants. “At the 38th International Sea Turtle Symposium in Kobe, On the final day of the Symposium, 23 February, the Banquet was Japan, on 20 February 2018, a panel of international sea turtle held in the Portopia Hotel’s Ballroom. A welcome speech by Kizou experts have taken an important step forward in discussing Hisamoto, Kobe Mayor, was followed by a sake barrel opening and issues surrounding the idea of moving beyond protection. The cheers with wooden square cups of sake. The evening proceeded panel members encouraged further dialogue on the need for with the Award Ceremony presenting the Archie Carr Student flexible and diverse conservation and management strategies Awards, the ISTS Career Awards, and the Grassroots Conservation in accordance with sea turtle population status, management Award. The formal portion of the evening closed with words of context, scientific knowledge, local and traditional knowledge, appreciation from the President and the ceremonial passing of the socioeconomic needs, and cultural considerations. In doing ISTS Presidential Trowel to incoming 2019 President Ken Lohmann. so, we commit to respecting the diversity in conservation and A spirited two hours of dancing with live band brought an end to management strategies and recognize that the path to thriving an intense yet relaxed week of activities. sea turtle populations may differ with each community, ISTS Career Awards. Thushan Kapurusinghe, ISTS Career culture, country, and region that have shared populations Awards Committee chair, and team members: Andres Estrades, of sea turtles. As the President of the 38th International Sea Shaya Honarvar, Michael Jensen and Erin Seney did an excellent Turtle Symposium, I declare this moment as the start of a job and presented this year’s meeting with an incredible group of new conversation to take us beyond protection of sea turtles.” awardees. ISTS Lifetime Achievement Awards were presented to *Personal statement by 2018 ISTS President, not intended to Maria Ângela (Neca) Marcovaldi from TAMAR in Brazil, Donna be taken as a resolution. Shaver of Padre Island National Seashore, Naoki Kamezaki of Student Committee. The Student Committee chaired by Itzel Okayama University of Science, and to Hiroyuki Suganuma of Sifuentes and Catalina Uruena conducted its 8th year of activities Everlasting Nature of Asia. “Colola: Capital Mundial de la Tortuga dedicated to welcome and encourage student attendees. This year Negra” in Mexico received the ISTS Champions Award. Kazuyoshi there was three core activities: Student Presentation Feedback during Omuta of Yakushima Umigame-Kan was awarded the Ed Drane which 70 evaluators volunteered to give feedback to 124 student Award for Volunteerism. President’s Awards were given to Yasuo presentations. The second activity was a half-day workshop “The Kondo for his pioneer work started at Hiwasa in 1950, and to Art of Writing Science,” which aimed to help students develop skills Team Minabe for its contribution to conservation and research of needed to write, submit, and publish scientific manuscript. Richard sea turtles. Reina, Jeff Seminoff, Kate Mansfield, and Sean Williamson kindly Archie Carr Student Awards. There were 39 student oral shared their experiences with 24 attendees. Lastly, with the aim to presentations and 78 student poster presentations nominated for the promote networking and communication among students and other Archie Carr Student Awards. Judges of the student presentations symposium participants, and also enhance their participation in the in Kobe were: Agnese Mancini, ALan Rees, Aliki Panagopoulou, Society, a Student Social Mixer was held on the Tuesday evening. Carlos Carreras, Hideaki Nishizawa, Jillian Hudgins, Joe Pfaller, The mixer included the “Speed Chatting with the Experts”. The Kate Mansfield, Katsufumi Sato, Kelly Stewart, Mark Hamann, lineup was: Tomo Eguchi, Irene Kelly, Nicolas Pilcher, Nancy Michael Jensen, Mick Guinea, Rupika Rajakaruna, Scott Whiting FitzSimmons, Takahiro Shimada, Kei Okamoto, David Booth, , and Simona Ceriani. Coordinators Matthew Godfrey and Andrea Michael Salmon, Simona Ceriani, Brian Shamblin, and Katherine Phillott presented eight students with Archie Carr awards for Comer Santos. outstanding presentations: Kennta Fujita (Biology winner), Sara Social Events. The social component of the symposium was Abalo Moral (Biology runner-up), Helen Pheasey (Conservation highlighted by the Welcome Social, Student Committee activities, winner) and MacKenzie Tackett (Conservation runner-up) won Japan Night, Silent and Live Auctions, as well as the Award in the Poster Category. Shohei Kobayashi (Biology winner), J. Ceremony and Banquet, and Field Trip. The Welcome Social Roger Brothers (Biology runner-up), Ryan Pearson (Conservation was held Monday evening at Suma Aqualife Park, during which winner) and Seh Ling Long (Conservation runner-up) won in the attendees were able to enjoy watching a variety of marine animals Oral Category.

Marine Turtle Newsletter No. 156, 2019 - Page 46 Grassroots Conservation Award. Now in its 8th year, Okinawa Churaumi Foundation & Aquarium, NYK Group, Nestle the Grassroots Conservation Award given to a poster or oral Japan, Sysmex, Kamihata Fish Industry Group, Chubu Doboku, presentation that best demonstrates a positive contribution towards George Balazs & Golden Honu Services of Oceania, US Fish and the conservation of marine turtles and/or their habitats went to Ning Wildlife Service, Wildlife Computers, and Lotek. At the Bronze Yen from Hiin Studio for their presentation “From Trash to Money: level (US$500-US$999): Native Vision, and Teikyo University of A Successful Case Combining Green Turtles Protection and Beach Science. At the Inconel level (US$100-US$499): Janet Hochella, Clean-up in Taiwan.” The judges were Ingrid Yanez, Jack Frazier, パシコ貿易株式会社, 株式会社オキナワマリンリサーチセン Angela Formia, Zahirul Islam, Manjula Tiwari and Muralidharan ター, 株式会社日本ドルフィンセンター, 紀宝町役場, 株式会 Manoharakrishnan. 社日本海洋生物研究所, 国民宿舎 紀州路みなべ, 堺市漁業 Travel Grants. Making the symposium accessible to students 協同組合, 洲崎神社, カロラータ株式会社, アースウォッチ・ and international participants is a major priority of the Society, and ジャパン, マイスター大学堂, 横浜商科大学, 椎名大敷組合, to this end travel grants are provided to offset the cost of attending. 三津大敷組合, 高岡大敷株式会社, 漁師のNPO, 名古屋港水族 Alexander Gaos chaired the Travel Grant Committee, along with 館, 浦嶋神社, 日映エンタープライズ株式会社, 南知多ビーチ the Regional travel chairs Angela Formia, Kelly Stewart, Karen ランド, うみまーる企画, いであ株式会社, 日和佐うみがめ博 Eckert, Andrea Phillott, ALan Rees, Alejandro Fallabrino, Aliki 物館カレッタ, hau’oli, キュービックアイ, 有限会社松仙ベッ Panagopoulou, and Emma Harrison. Through their coordinated 甲製作所, 株式会社モンベル, ITストアーMANATO, 特定非営 efforts the ISTS was able to support a total of 127 overseas travel 利活動法人宮崎野生生物研究会, 西大和学園中学校・高等学 grant applicants with full lodging during the symposium and 50 校, 大本山 須磨寺, 株式会社串本海中公園センター, ホクト Japanese students partially. The distribution of bed grants per region 環境システム株式会社, 日本ミクニヤ株式会社, and 恋の浦ウ was as follows: 9 to Africa representatives, 25 to Asia Pacific, 3 to ミガメの会. At the Monel level (up to US$99): 株式会社神戸ゴ Caribbean, 21 to Europe, 17 to Mexico & Central America, 12 to マルゴ, 門井社会保険労務士事務所, コマタニ商会, ペンショ South America, 9 to South Asia, 4 to Middle East & North Africa, ンむぎわらぼうし, 株式会社西尾製作所, 株式会社吉高屋, 谷 and 27 to US & Canada. In accordance with some Japanese sponsor 内FP保険事務所有限会社, させぼパールシー株式会社, 神戸動 wishes, the symposium allocated US$7,800 in cash awards to 植物環境専門学校, 小学館, 紀伊半島ウミガメ情報交換会, 国 applicants from Asia and the Pacific. 立公園成ヶ島を美しくする会, 料亭花月, 須磨ふるさと生きも Board of Directors Meeting. The Board of Directors meeting のサポータ, 水中カメラ専門店 海の写真屋さん, アクアワー was held on Tuesday, 20 February. The meeting was fruitful and ルド茨城県大洗水族館, 株式会社アドバンス, 志摩半島野生動 lasted until midnight. The Board received and discussed reports 物研究会, 江崎グリコ株式会社, すさみ海立エビとカニの水族 from the Nominations Committee, ISTS Career Awards Committee, 館, 株式会社ビデオエイペックス, 特定非営利活動法人Turtle Students Awards Committee, Student Committee, Travel Grant Crew, 琴引浜鳴き砂文化館, 有限会社浦田帆屋, 有限会社月灘 Committee, as well as reports from the Treasurer. 屋, 南浦はくせい店, 有限会社ウミガメフーズ, 図書出版 南方 ISTS Business Meeting. The 2018 ISTS Business Meeting was 新社, and 株式会社 海の中道海洋生態科学館 held on Friday, 23 February. ISTS President Yoshimasa Matsuzawa Exhibitors and Vendors. The exhibitors and vendors that called the meeting to order, and reports were provided by Treasurer participated in the Kobe symposium were: CLS America, Inc.; (George Balazs), Travel Grant Committee (Alexander Gaos), 4K-UHD Deep Sea Camera System (Kanso Co. Lyd.); Lotek Nominations Committee (Kate Mansfield) and Students Committee Wireless Inc.; Telonics, Inc.; Wildlife Computers; Bioko Marine (Itzel Sifuentes). Other issues related to our Society also were Turtle Program; Everlasting Nature of Asia (ELNA); Hiin Studio; discussed. No Resolutions were submitted for consideration at this Marinelife Alliance (MLA); Pro Delphinus; Taiwan Sea Turtle Symposium. Ken Lohmann, 2019 ISTS President, provided details Conservation Society; Turtle Crew; TurtleSpot in Taiwan; The State regarding the next year’s symposium to be held in Charleston, South of the World’s Sea Turtles (SWOT); and Japan Bekko Association. Carolina, USA. The theme of next year’s meeting is “Navigating the Going Green. The ISTS made efforts to minimize waste, Future.” Dates have been set as 2-8 February 2019, during which including use of the mailing list, ISTS website and various social time Society members will once again get together to celebrate sea network service. Participants were strongly encouraged to bring turtles. their own mug for coffee break. Paper cups prepared for those ISTS Elections. As a result of the 2018 Society’s annual election, who did not bring their own mug were made from forest thinning Diego Amorocho from Colombia was elected President for the ISTS products. Instead of paper or plastic bags, a Japanese traditional symposium in 2020. Also, the elections added two new members wrapping cloth was used for a participant package. During Japan to the Board of Directors (year indicates board member’s end of Night, symposium participants had the opportunity to train how to term): Andres Estrades (2023) and Richard Reina (2023). Sheryan fold and use the wrapping cloth. Aquarium staff sorted waste one Epperly and Irene Kelly were elected to join the Awards Committee. by one after any social events. Funding. Generous funding by many entities made the success Acknowledgments. Organizing the Kobe symposium took a large th of the 38 symposium possible. The organizing committee deeply number of volunteers allocated to various committees: registrars, thanks the following donors for their generosity. At the Platinum fundraising, program, sessions, poster, workshop, student, travel level (US$25,000 and above): Mitsubishi Heavy Industries, and grants, awards, exhibitor, volunteer, auction, visitor visa application Suma Aqualife Park. At the Gold level (US$10,000-US$24,999): support, communications, and proceedings. All of these individuals Osaka College of ECO & Animals, Lion Corporation, and Sea gave a significant number of hours, effort and dedication towards Turtle Association of Japan. At the Silver level (US$1,000- their entrusted tasks. By alphabetical order of their first name, the US$9,999): Kanetetsu Delica Foods, Stella Chemifa, Orgabits, Society thanks: Agnese Mancini, Akira Oda, ALan Rees, Alejandro Marine Turtle Newsletter No. 156, 2019 - Page 47 Fallabrino, Alexander Gaos, Alexandre Girard, Alexis Guilleux, Baba, Kojiro Mizuno, Lalith Ekanayake, Laura Gibbons, Mai Alexis Gutierrez, Aliki Panagopoulou, Andrea Phillott, Andrew Takase, Manjula Tiwari, Marc Girondot, Marina Zucchini, Mario DiMatteo, Andrews Agyekumhene, Andy Estrades, Angela Formia, Mota, Mark Hamann, Matthew Godfrey, Michael Jensen, Michael Antonio Di Bello, Ayaka Asada, Asuka Ishizaki, Brendan Godley, Salmon, Mick Guinea, Misako Munechika, Moe Wajiki, Momoyo Brian Shamblin, Cali Turner Tomaszewicz, Camryn Allen, Carlos Muramoto, Motoki Sugiura, Muralidharan Manoharakrishnan, Carreras, Catalina Uruena, Chiho Kezuka, Colin Limpus, Connie Nancy Fitzsimmons, Naoki Koga, Natalie Wilderman, Neca Ka-Yan Ng, Daisuke Shiode, Daniel Gonzalez-Paredes, Daniela Marcovaldi, Nicolas Pilcher, Paolo Casale, Richard Reina, Rod Freggi, Dave Owens, David Booth, Emma Harrison, Erin Seney, Mast, Rupika Rajakaruna, Sandra Hochscheid, Satomi Kondo, Saya George Balazs, George Shillinger, Hector Barrios-Garrido, Heather Hirai, Scott Whiting, Sean Williamson, Shaya Honarvar, Shigetomo Harris, Hideaki Nishizawa, Hideo Hatase, Hiroyuki Suganuma, Hirama, Simona Ceriani, Sophie Baudel, Takahide Sasai, Takahiko Hiroyuki Yoshida, Ingrid Yañez, Irene Kelly, Isao Kawazu, Itzel Ide, Takahiro Shimada, Takashi Ishihara, Takuya Fukuoka, Tatsuya Sifuentes, Jack Frazier, Jacques Fretey, Jane Provancha, Jean- Oshika, Thushan Kapurusinghe, Tomo Eguchi, Tomoka Eguchi, Michel Guillon, Jeanette Wyneken, Jeff Seminoff, Jesus Tomas, Tomoka Higuchi, Tomoko Hamabata, Tomoko Narazaki, Tomotomi Jillian Hudgins, Joanna Alfaro, Joe Pfaller, John Wang, Junichi Saito, Tsung-Hsien Li, T. Todd Jones, Vanessa Bezy, Yakup Kaska, Okuyama, Karen Eckert, Kartik Shanker, Kate Mansfield, Katherine Zahirul Islam, and the various volunteers that were assigned on-site. Comer Santos, Katsufumi Sato, Kazunari Kameda, Kei Okamoto, Also, the symposium would not have been possible without the Kelly Stewart, Kensuke Matsumiya, Kiyomi Nakamura, Koji support from the donors mentioned above.

Figure 1. Top: Special session on “Beyond Protection of Sea Turtles.” Bottom: Traditional calligraphy demonstration during the “Japan Night” social event. Marine Turtle Newsletter No. 156, 2019 - Page 48 RECENT PUBLICATIONS This section consists of publications, books, reports, and academic theses that feature subject material relevant to marine turtles. Most references come from major search engines, and the editors encourage authors to submit their publications directly by email to the Recent Publications editor: [email protected].

ABALO-MORLA, S., A. MARCO, J. TOMÁS, O. REVUELTA, E. AMAYA, O., R. QUINTANILLA, B.A. STACY, M.Y.D. BOTTEIN, ABELLA, V. MARCO, J.L. CRESPO-PICAZO, C. FERNÁNDEZ, L. FLEWELLING, R. HARDY, C. DUEÑAS & G. RUIZ. 2018. F. VALDÉS, M.C. ARROYO, S. MONTERO, C. VÁZQUEZ, J. Large-scale sea turtle mortality events in El Salvador attributed EYMAR, J.A. ESTEBAN, J. PELEGRÍ & E.J. BELDA. 2018. to paralytic shellfish toxin-producing algae blooms. Frontiers in Survival and dispersal routes of head-started loggerhead sea turtle Marine Science 5: 411. (Caretta caretta) post-hatchlings in the Mediterranean Sea. Marine ANANDHI, A., A. SHARMA & S. SYLVESTER. 2018. Can Biology 165: 51. meta-analysis be used as a decision-making tool for developing ABELLA, E., R.M. GARCÍA-CERDÁ & A. MARCOL. 2017. scenarios and causal chains in eco-hydrological systems? Case Estimating the fertilization rate of sea turtle nests: comparison study in Florida. Ecohydrology 11: e1997. of two techniques. Basic and Applied Herpetology 31: 33-44. ARCHIBALD, D.W. & M.C. JAMES. 2018. Prevalence of visible AGUILERA, M., M. MEDINA-SUÁREZ, J. PINÓS, A. LIRIA- injuries to leatherback sea turtles Dermochelys coriacea in the LOZA & L. BENEJAM. 2018. Marine debris as a barrier: Northwest Atlantic. Endangered Species Research 37: 149-163. Assessing the impacts on sea turtle hatchlings on their way to the ARIEL, E., F. NAINU, K. JONES, K. JUNTUNEN, I. BELL, J. ocean. Marine Pollution Bulletin 137: 481-487. GASTON, J. SCOTT, S. TROCINI & G.W. BURGESS. 2017. AGUSTIN, H., D. SUPRIADI & D.R. HIDAYAT. 2018. Digital Phylogenetic variation of chelonid alphaherpesvirus 5 (ChHV5) in marketing in unsustainable wildlife tourism (a study on the populations of green turtles chelonia mydas along the Queensland practice of marketing communication of sea turtles observation Coast, Australia. Journal of Aquatic Animal Health 29: 150-157. tourism). 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Marine Turtle Newsletter No. 156, 2019 - Page 68 Crawls and body pits made from nesting green sea turtles on Long Beach, Ascension Island. Photo: M. Godfrey

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