Post-Nesting Migrations Patterns of Green Turtles (Chelonia Mydas) from the Egyptian Red Sea Omar Attum1*, Andrew Kramer1, Tamer Mahmoud2, Moustafa Fouda3

Zoology in the Middle East, 2014 http://dx.doi.org/10.1080/09397140.2014.962833

Post-nesting migrations patterns of Green Turtles (Chelonia mydas) from the Egyptian Red Sea Omar Attum1*, Andrew Kramer1, Tamer Mahmoud2, Moustafa Fouda3

1Department of Biology, Indiana University Southeast, New Albany, USA. 2Wadi El Gemal Na- tional Park, Egyptian Environmental Affairs Agency, Maadi, Cairo, Egypt. 3Ministry of State for Environmental Affairs, Cairo, Egypt.

(Received 1 July 2014; accepted 23 August 2014) In order to identify the migratory pathways and foraging grounds of post-nesting Green Turtles (Chelonia mydas) in the Red Sea, we attached satellite transmitters to four females immediately after egg deposition and tracked them between 207 and 647 days. We identified four geographically distinct post-nesting habitat areas and migration paths from Zabargad Island, Egypt which was remarkable given our small sample size. Our shortest migration was 140 km and the longest 940 km, with the migrations and post-nesting habitat encompassing the boundaries of four of the seven Red Sea countries (Egypt, Sudan, Eritrea, and Saudi Arabia). The post-nesting habitats were located in shallow coastal habitat and three consisted of near-shore archipelagos. Two turtles moved past areas of suitable post-nesting habitat that was occupied by other turtles, which suggests that these turtles may be exhibiting fidelity to certain feeding and nesting sites. Our results suggest that regional and multi-national cooperation will be needed to protect sea turtles that nest on Zabargad Island, a nesting site that is important for Egypt and other Red Sea nations. Keywords: Egypt, Green Turtles, off-shore beaches, sea turtles, migration.

Introduction The Red Sea is known for its high marine biodiversity and has been suggested to be an important nesting site for sea turtles despite the sea’s small size and relative isolation from other marine waters (Frazier & Salas, 1984). Five species of sea turtles have been recorded in the Red Sea, with only the Hawksbill Turtle, Eretmochelys imbricata, and the Green Turtle, Chelonia mydas, being regularly observed and known to nest (Frazier & Salas, 1984; Frazier, Bertram & Evans, 1987; Hanafy, 2012). Green Turtles are a

Downloaded by [UAE University] at 09:18 12 September 2014 globally endangered species that have many natural history traits that make the species vulnerable to anthropogenic disturbance (Godley et al., 2008, IUCN, 2011). These include delayed sexual maturity, ontogenetic habitat use, and undertaking of long migrations that utilize spatially distant and different habitats (Godley et al., 2008, Musick & Limpus, 1997, Seminoff et al., 2008). In addition, the habitats of sandy beaches that are used as nesting grounds and sea grass beds that are utilisaed as feeding areas are com- monly degraded and the availability of these habitats is decreasing as a result of anthropogenic disturbances (Short et al., 2011). Very little is known about the Green Turtle population or their ecology in the Red Sea, with the exception of the distribution of nesting sites (Frazier & Salas, 1984; Fra- zier et al., 1987; Hanafy, 2012; Miller, 1989). It is estimated that the nesting population in the Red Sea comprises around 1,500 females per year (as referenced in Hanafy, 2012)

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and that females may lay up to four nests during the nesting year, which occur every three or more years (Miller, 1989). Population modeling has suggested that conservation of adult females, which have delayed sexual maturity and are long-lived, are vital to the viability of sea turtle populations (Heppell, Crouse, & Crowder, 2002). The identifica- tion of post-nesting migration routes provides valuable information about the life history of sea turtles such as location of nesting sites, feeding grounds, migration routes between different habitats, how movement relates to political boundaries, and potential threats to turtles (Amorocho, Abreu-Grobois, Dutton & Reina, 2012; Hays et al., 2002; Hamman et al., 2010; Maxwell, 2011; Rees, Jony, Margaritoulis, Godley, 2008). Under- standing the many factors that contribute to the use of dynamic seascapes is needed to make informed management decisions to assist in the conservation of sea turtles (God- ley et al., 2008). The objective of this study was to begin to identify the migratory pathways and foraging grounds of post-nesting Green Turtles in the Red Sea.

Material and Methods Study Area. The Red Sea is a relatively small sea (437,900 km2) and is connected to the tropical Indian Ocean through the narrow Straits of Bab al Mandab. The offshore beaches of the Red Sea islands are important nesting grounds for sea turtles (Frazier et al., 1987; Hanafy, 2012) and the offshore beaches of Zabargad Island (23°60’N, 36°20’E) are believed to be the largest nesting site for Green Turtles within the Egyptian boundaries of the Red Sea (Hanafy, 2012). Zabargad Island (470 ha) mostly consists of metamorphic rock hills and is located 70 km from the mainland, while within the boundaries of Elba Protectorate. The nesting season occurs between June to August with the yearly number of nests ranging from 438–1527 (Hanafy, 2012). Transmitters. We attached Sirtrack KiwiSat 101 satellite transmitters (18 cm x 6 cm, 500 g) to four female Green Turtles, which we refer to as Fahd, Nada, Sallam, and Rasheeda, immediately after egg laying on the southeastern beaches of Zabargad Island on 25 July 2010. The transmitters were attached to the highest point on the carapace following standard procedures (Luschi, Hays, del Seppia, Marsh, & Papi, 1998). Prior to transmitter attachment, the anterior carapace was sand- ed and cleaned. The transmitters were attached to the carapace with epoxy and covered with an additional layer of marine putty. Transmitters were set to record location data once every 48 hours. Transmitters were active between 207 and 647 days (Table 1) Tracking. We used the ARGOS system to estimate the turtles’ locations and the Satellite Track- ing and Analysis Tool (STAT) to interpret and filter the data (Coyne & Godley, 2005). The AR- GOS data were analysed using the least-squared algorithm. In order to improve the accuracy of the data, we filtered the data to contain only data points from ARGOS estimated accuracy location classes 3 (<150 m), 2 (150–350m), 1 (350–100m), and A (no estimate of location accuracy) (Hays

Downloaded by [UAE University] at 09:18 12 September 2014 et al., 2001). In addition, we removed data points further than 100 km from the previous location, data points that indicated turtle speed greater than 5 km/h (Broderick, Coyne, Fuller, Glen, & Godley, 2007; Tröeng, Dutton, & Evans, 2005), data points that were recorded at greater than 2 m above sea level, and locations that were over land. All data points were imported into ArcMap 10.1 for analysis. Data points were classified as nesting, migration, or post-nesting habitat. Nesting points were defined as all points from transmitter attachment to until the first migration point. Migration was defined as beginning at the first data point away from Zabargad Island that was followed by con- secutive points moving in the direction away from the island. Minimum migration distance was measured by adding the distances between each migration point for each turtle. Post-nesting habitat was defined as locations after migration ceased, indicating that the turtle was residing within a general area for several weeks (Hays et al., 2002). Home Range Analysis. We used ArcMap 10.1 to determine the turtles’ home ranges within their feeding grounds. The ARGOS data points were first loaded into ArcMap10.1 and their coordinate systems were converted from geographic coordinates to UTM WGS84 zone 36N for Nada and

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Table 1. Migration distances, transmission activity, and home range areas of post-nesting Green Turtles in the Red Sea. Nada 1 represents the first migration route to post-nesting habitat and Nada 2 represents the second migration route of this individual. We were not able to estimate activity range sizes for the Nada 2 route because the transmitter ceased to send signals during the course of the second migration.

Migration & Home Range Minimum Migration KernelArea (km2) MCP Area Turtle Distance (km) 50% 95% (km2) Fahd 140 28.88 249.99 793.93 Nada 1 150 22.16 172.30 410.72 Nada 2 610 Sallam 940 113.98 1095.08 1381.69 Rasheeda 550 21.04 212.68 1560.61 Mean±SE 404±173 46.52±22.6 432.5±212 1036.7±265 Transmission Activity Total Transmission Total Data Points Total Filtered Data Turtle Activity (days) Points Fahd 397 279. 191 Nada 207 354. 231 Sallam 237 291. 212 Rasheeda 647 361. 289 Mean±SE 372±87.2 321±21.1 211±11.6

Rasheeda’s respective feeding grounds and to UTM WGS84 zone 37N for Fahd and Sallam’s respective feeding grounds. We calculated home range area as a minimum convex polygon. To limit the effect of outliers on home range area, we also used the Geospatial Modeling Environ- ment (Formerly Hawth’s Analysis Tools) to calculate the 50% & 95% fixed kernel density polygons for each turtles’ home range (Beyer, 2012, R Core Team, 2013). Bandwidth was calculated separately for each turtle using the plug-in bandwidth selector (Jones, Marron, & Sheather, 1996). Any portion of the kernel density estimates that fell on land were not included in the area calcula- tion.

Results Downloaded by [UAE University] at 09:18 12 September 2014 The mean curved carapace length of the four turtles was 105+6.0 cm and their mean clutch size was 111+5 eggs. We obtained 279 locations and were able to use 88 locations after data filtering for Fahad, obtained 354 locations and used 123 locations for Nada, obtained 291 locations and used 79 locations for Sallam, and obtained 361 locations and used 72 locations for Rasheeda (Table 1). All four turtles migrated from Za- bargad Island toward the western coastline of the Red Sea and continued their journeys in the four different directions of varying lengths (Figure 1). Fahd remained around Zabargad Island for about 30 days before beginning migration. Once migrating, she initially traveled WSW, toward the coast, but then began a rapid southern path reaching her foraging grounds in the near shore Siyal archipelago along the Egyptian coast and within the boundaries of Elba protectorate about 5 days after the first recorded migration location (Figure 1). During the course of her migration, Fahd was located a mean distance of 37+7.9 km from the coastline, and her minimum migration distance was 140 km. The last signal was received on 26 August 2011. 4 O. Attum et al.

Figure 1. Minimum migration paths of the four turtles – Fahd, Nada, Sallam, and Rasheeda – from Zabargad Island, as determined by STAT filtering their respective data points. The polygons represent the minimum convex polygon areas for each individual’s foraging grounds.

Nada remained within the vicinity of Zabargad Island for about 55 days and then began a relatively straight NW path to her feeding grounds near the Egyptian fishing village of Abu Ghusun, which is within the boundaries of Wadi Gemal National Park Downloaded by [UAE University] at 09:18 12 September 2014 (Figure 1). Her migration lasted about 10 days, and her minimum migration distance was 150 km. During Nada’s migration she was located a mean distance of 26+7.6 km away from the coast. Nada resided in Wadi Gemal National Park for about 115 days and then began a second migration towards Saudi Arabia, traveling first ENE, then NW, then SW, then ESE, then SE, and finally SSE (Figure 1). This convoluted path continued for about 14 days before we stopped receiving her signal about 90 km south of Yanbu, Saudi Arabia. The minimum migration distance of this second migration was 610 km and the mean distance from the coast was 77+3.0 km. Nada’s last data point

was recorded on 17 February 2011, only 172 km away from Zabargad Island. Sallam remained within the vicinity of Zabargad Island for about 10 days before beginning her migration. Her minimum migration distance was 940 km as she traveled south along the western coast of the Red Sea, passing through the territorial waters of three Red Sea nations, Egypt, Sudan, and Eritrea (Figure 1). She reached her feeding grounds on the northern periphery of Dahlak Archipelago off the coast of Eritrea in Zoology in the Middle East 5

about 25 days. During the course of her migration she was located a mean distance of 26+4.2 km away from the coast. The last location was recorded on 12 April 2011. Rasheeda began directional movement almost immediately after transmitter attachment. She travelled north, closely following the western coast of the Red Sea with a maximum distance of 11 km away from the coast and a mean distance of 5+3 km. She reached her feeding grounds in the Gulf of Gamsha and nearby the Gamsha archipelago, 60 km northwest of the resort city Hurghada, after about 40 days and a minimum migration distance of 550 km (Figure 1). We continued receiving satellite signals within her feeding grounds until 2 May 2012. The turtles’ home ranges were of widely disparate sizes (Table 1). The minimum convex polygon area of the respective home ranges varied from 411 km2 to 1561 km2, mean 1037+265 km2 (Table 1). The 95% kernel densities ranged from 172 km2 to 1095 km2, mean 433±221 km2 and the 50% polygon areas ranged from 21 km2 to 114 km2, mean 47±23 km2.

Discussion While the sea turtles in our study moved along the coast as expected (Godley et al., 2008), we identified four geographically distinct migration paths and post-nesting habitat, which was remarkable given our small sample size (Whiting, Long, & Coyne, 2007). Our shortest migration was 140 km and the longest 940 km, with turtles migrating west, east, north, and south of the nesting sites. The migrations and post-nesting habitats encompassed the boundaries of four – Egypt, Sudan, Eritrea, and Saudi Arabia – of the seven Red Sea nations. The post-nesting habitats encompassed shallow coastal habitat and three were near-shore archipelagos. One turtle appeared to use more than one feeding ground as part of her migration towards Saudi Arabia. Some sea turtles are known to not take the most direct route to their destination, but instead utilise long rest- ing stops or multiple feeding grounds as part of their migration (Whiting et al., 2007). Two turtles moved through areas of suitable post-nesting habitat that was occupied by other turtles, which suggests that these turtles may be exhibiting fidelity to certain feeding and nesting sites (Broderick et al., 2007; Hays et al., 2002). For example, turtle Sallam, moved over 900 km south to the Dahlak archipelago passing a potential post- nesting habitat utilised by another turtle in this study. In addition, this individual could have also travelled less than 100 km south to nest on any of the numerous beaches of Dahlak archipelago, a known nesting spot for Green Turtles in the Red Sea (Frazier et al., 1987). The variation in foraging and nesting site selection could be the result of Downloaded by [UAE University] at 09:18 12 September 2014 unknown disturbances to closer nesting or feeding sites or may simply be an evolution- ary strategy to maintaining sea turtle populations over geologic time scales (Seminoff et al., 2008). This variation would be advantageous by allowing some sea turtles to escape catastrophic oceanographic events that affect nesting frequency and availability (Semi- noff et al., 2008). Our results corroborate previous studies that suggest Zabargad Island is an important nesting site for Green Turtles in the Red. Islands may represent important nesting habitat for sea turtles and other wildlife because offshore beaches are believed to have fewer natural predators and experience less anthropogenic disturbance than mainland nesting sites as a result of their isolation. The Red Sea islands in the territorial waters of Egypt are also afforded some protection as a result of their remoteness, falling within the boundaries of marine protected areas, and subjected to military control that limits visitor access (Hanafy, 2012). The mainland beaches of the Egyptian Red Sea are intrinsically more vulnerable as a result of relative accessibility to humans that has resulted in rapid- 6 O. Attum et al.

ly growing beachfront development, recreational use, and other anthropogenic disturbance that has contributed to the declining nesting of Green Turtles on Egypt’s mainland beaches (Hanafy, 2012). The conservation value of island nesting sites, such as Zabar- gad, will presumably increase as mainland beaches continue to experience growing degradation and coastal development. Effective long-term management of Green Turtles will require additional studies with greater sample sizes that address the numerous threats to the biodiversity of the Red Sea. Maintaining the connection between feeding grounds and nesting sites of the geographically distinct mainland beaches, near shore islands, archipelagos, and isolated islands should remain a priority to increase survival during different life history periods. Egypt’s marine protected areas provide legal protection to Zabargad Island, a portion of the migration route, and some of the post-nesting habitat identified in this study. How- ever, the migration routes and post-nesting habitats of most of the turtles in our study did not fall under the protection of marine protected areas. Sea turtle protection within Egypt’s marine protected areas is challenging as a result of numerous challenges such as pollution, overuse of areas as recreational sites, illegal fishing, and unknown levels of sea turtle bycatch from local community fishermen (Fra- zier & Salas, 1984, Samy, Sanchez Liasco, & Forcada, 2011, Rouphael, Abdulla, At- tum, Marshall, & Ghazali, 2013). The Red Sea is also an important source of oil and waterway marine transportation, whose activities contribute to degradation of the marine ecosystems through oil spills, discharge from tankers and oil exploration through submarine explosions and marine transportation (Frazier et al., 1987, Miller, 1989). For example, the Gulf of Gamsha, the post-nesting habitat of Rasheeda, was the site of two relatively extensive oil spills in 2010 and 2011. Rasheeda appeared to survive the im- mediate spills, but the long term effects on the habitat or survival of the turtle are unknown. The multinational spatial scale could potentially increase the difficulty in effec- tively conserving sea turtles in the Red Sea. The females that nested on Zabargad Island utilized migration routes and post-nesting habitats that include coastal areas and archipelagos of four Red Sea nations. Regional and multi-national cooperation will be needed to protect sea turtles that nest on Zabargad Island.

Acknowledgements We would like to thank the rangers of Red Sea National Parks and Egyptian Environmental Af- fairs Agency for their support and assistance. We are also grateful for the assistance provided by Waheed Salama, Mohammed Abbas, David Taylor, Jon Norman, and the Indiana University

Downloaded by [UAE University] at 09:18 12 September 2014 Southeast Field Biology class. This research was funded by Indiana University Southeast.

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