J. C. Báez 1,2*, D. Macías 1, J. J. Bellido 3, J. A. Camiñas 1

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1 Vie et milieu - Life and environment, 2017, 67 (1): 1-5 Differential temporal and spatial distribution of adult loggerhead sea turtles from Gulf of Cádiz to western Mediterranean Sea J. C. Báez 1,2*, D. Macías 1, J. J. Bellido 3, J. A. Camiñas 1 1 Instituto Español de Oceanografía, Centro Oceanográfico de Málaga, Spain 2 Investigador asociado de la Facultad de Ciencias de la Salud, Universidad Autónoma de Chile, Chile 3 Aula del Mar de Málaga, Málaga, Spain * Corresponding author: granbaez_29@hotmail.com SEA TURTLE BY-CATCH STRANDING MEDITERRANEAN SEA MIGRATION ABSTRACT. The aim of this paper was to search for and model spatial and seasonal trends in occurrences (stranding or by-catches) of adult loggerhead turtles in the western Mediterranean area and Gulf of Cádiz (Atlantic) independently of their origin. Adult turtles were only bycaught on longlines from May to August. Adults were stranded in the eastern and western areas of the Strait of Gibraltar threshold throughout the year. In the Gulf of Cádiz (Atlantic), strandings were significantly concentrated in May and June, whereas in the Alboran Sea (Mediterranean), strandings mainly occurred in June and July. The probability of catching a mature loggerhead increases during June and July south of the Balearic Islands. The results suggest that adult loggerhead turtles move (migrate) from the Atlantic area (Gulf of Cádiz) to the Mediterranean (Alboran Sea) from May to June, and subsequently move to the Balearic Sea from June to July. These results are in line with those obtained by previous studies. INTRODUCTION Sea turtles have relatively high fecundity and low natural mortality during the adult phase (Musick 1999). In contrast, immature individuals (hatchlings and juveniles) present high natural mortality rates (Wallace et al. 2008). For this reason, mature-phase mortality due to fisheries has a higher impact on sea turtle populations than nonnatural immature-phase mortality (Wallace et al. 2008). By-catch in longline fisheries is considered to be a critical global threat to loggerhead turtles Caretta caretta (Linnaeus, 1758) (Lewison et al. 2004), and is particularly severe in the Mediterranean Sea (Camiñas et al. 2006, Báez et al. 2007a,b). According to recent studies, bycatch frequency and size differentiation of loggerheads is a function of surface longline gear-type (e.g. Báez et al. 2013). Thus, in the Western Mediterranean, surface longliners targeting albacore (LLALB) using smaller hooks tend to capture smaller loggerheads, but have the highest by-catch per unit of effort (BPUE), whereas other longliners, such as traditional surface longliners targeting swordfish (LLHB) using larger hooks tend to capture larger animals; moreover, LLHB have the lowest BPUE (Báez et al. 2013). In the western Mediterranean, loggerhead sea turtle specimens from the Mediterranean, Northeast American, and Cape Verde populations are present (Monzon-Arguello et al. 2010). The western Mediterranean contains loggerheads in different life stages (mainly subadults). They are captured as by-catch in several fisheries: driftnets (Silvani et al. 1999, Tudela et al. 2005), drifting longlines (Camiñas 1988, Aguilar et al. 1995, Camiñas & Valeiras 2001, Báez et al. 2007a,b), bottom trawling (Casale et al. 2004), and trammel nets (Carreras et al. 2004, Lozano et al. 2011); however, there is a lack of reliable information on the relative contribution of each fishing gear to the total by-catch. Other gears that affect total mortality in sea turtles have been evaluated by Álvarez de Quevedo et al. (2010). Although some nests are present in the western Mediterranean (Bellido et al. 2015), nesting grounds for the Mediterranean loggerheads concentrate in the eastern basin (Margaritoulis et al. 2003). The Balearic Sea is considered a foraging area for immature and subadult loggerheads; individuals from the three mentioned populations from the Mediterranean Sea and Atlantic Ocean converge in this area (see for example, Camiñas & de la Serna 1995). The recent observations of nesting loggerheads in the Western Mediterranean have revived a debate about the use of the Iberian Peninsula coast as a recurrent nesting area for loggerheads (Tomás et al. 2002, 2008, Bellido et al. 2015). Unfortunately, neither regular net monitoring, nor rigorous studies on the abundance and distribution of adult individual loggerheads in this area have been conducted on Spanish beaches. The aim of the present article was to look for spatial and seasonal trends in occurrences (stranding or bycatches) of adult loggerhead turtles in the western Mediterranean area and contiguous Gulf of Cádiz (Atlantic), independently of their origin.

2 2 J. C. BÁEZ, D. MACÍAS, J. J. BELLIDO, J. A. CAMIÑAS MATERIAL AND METHODS Data were collected from two different sources. Firstly, for the period from 1997 to 2013, we used monthly stranding data on adult loggerhead specimens (i.e. over 70 cm straight carapace length (SCR)) for both sides of the Strait of Gibraltar: the Gulf of Cádiz (Atlantic Ocean) and the Alboran Sea (Mediterranean Sea). For further details of stranding data monitoring, see Bellido et al. (2010a,b) (Fig. 1). This dataset provided information on 53 stranded loggerheads over 70 cm SCL (Straight Carapace Length) (Table I). Secondly, we used a set of monthly data on adult loggerhead by-catch (i.e. SCR > 70 cm) in Spanish surface longline fisheries operating from south of the Balearic Sea to the Strait of Gibraltar, between 0º to 1º longitude and 37º of latitude (Fig. 1). The size of the turtles by-caught in longline surface is difficult to take, because delaying maneuver fishing could result in damage and injury to the turtle. However, from 1999 to 2004, we did great effort to measure the turtles by-caught. We analyzed the spatial and seasonal distribution of 378 individual loggerheads with a known SCR, of which 23 were adult specimens, caught in LLHB (Table II). For further details on by-catch data, see Báez et al. (2013). Data analysis: We tested the monthly frequency of loggerhead stranding and by-catches using a chi-squared test (Sokal & Rolhf 1995). We also modelled the probability of catching at least one adult sea turtle using the following independent variables: period (months), and latitude and longitude (spatial-temporal factors). We performed forward stepwise binary logistic regression, which is a widely used technique to examine relationships between environmental independent variables and the probability of response of target variables (see, for example, Báez et al. 2007b, 2011). We used binary logistic regression to estimate the probability of by-catching an adult loggerhead in LLHB versus the independent variables: latitude, longitude, and period (months). Consequently, we assigned the value 1 when LLHB captured an adult loggerhead in a particular set, and assigned the value 0 when there were no captures. To validate the model, we assessed its goodness-of-fit using the Hosmer & Lemeshow test (Hosmer & Lemeshow 2000). We also assessed its discrimination capacity by applying the area under the receiving operating characteristic curve (AUC) method (Legendre & Legendre 1998, Hosmer & Lemeshow 2000, Lobo et al. 2008). RESULTS We observed that only adult specimens were bycaught on longlines from May to August. Adults were stranded on the eastern and western areas of the Strait of Gibral- Fig. 1. Detail of the study area. We plotted the strandings and bycatch areas of adult loggerhead turtles per season. Key: square, winter; Star, spring; Circle, summer; Rhombus, autumn.

3 DISTRIBUTION OF ADULT LOGGERHEAD SEA TURTLES FROM SOUTH OF SPAIN 3 Table I. Information on 53 stranded loggerheads over 70 cm SCL (Strait Carapace Length) from Andalucía coast. Province Month Year SCL Almería Cádiz Cádiz Cádiz Almería Cádiz Málaga Málaga Málaga Málaga Málaga Cádiz Cádiz Málaga Cádiz Cádiz Málaga Cádiz Cádiz Cádiz Cádiz Huelva Málaga Málaga Cádiz Cádiz Cádiz Province Month Year SCL Cádiz Huelva Huelva Málaga Málaga Málaga Almería Almería Almería Cádiz Huelva Málaga Málaga Cádiz Cádiz Cádiz Málaga Málaga Cádiz Huelva Málaga Málaga Huelva Almería Cádiz Cádiz Table II. Information on 23 by-caught loggerheads over 70 cm SCL (Straight Carapace Length). Key: LAT, Latitude; LONG, Longitude; Month, by-catch month; Year, by-catch year. LAT LONG Month Year SCL tar threshold throughout the year. In the Atlantic Gulf of Cádiz, strandings were significantly concentrated in May and June (Chi^2 = 82.34, P < 0.01, df = 11), whereas in the Mediterranean Alboran Sea, area strandings were significantly concentrated in June and July (Chi^2 = 62.74, P < 0.01; df = 11). In the easternmost part of the south Balearic Sea area, adult loggerhead by-catch was significantly concentrated in June and July (Chi^2 = 82.34, P < 0.01, df = 3). The logistic binary model showed that the probability of by-catching a mature loggerhead in LLHB was significantly associated with the independent variables latitude, longitude, and period (June, July). The model s goodness-of-fit was significant according to the Omnibus test (Omnibus test = , df = 4, P < ; Hosmer & Lemeshow test = 4.253, df = 4, P = 0.373) and showed outstanding discrimination capacity (AUC = 0.935). According to these results, the probability of catching a mature loggerhead increases during June and July in the area south of the Balearic Islands. DISCUSSION Our results suggest that adult loggerhead turtles move from the Gulf of Cádiz (Atlantic) to the Alboran Sea (Mediterranean) from May to June, and subsequently move to the Balearic Sea from June to July. These results are in line with those obtained by Camiñas & Serna (1995) and Camiñas (1997) based on fishing and by-catch data. Thus, adult loggerhead turtles from Atlantic nesting beaches migrate to the Mediterranean Sea through the Strait of Gibraltar during spring and summer. According to Carreras et al. (2015), two sporadic nesting events on the Spanish Mediterranean coast were originated by turtles born on Atlantic and Mediterranean nesting beaches, respectively. There has been recent discussion on the origin of loggerhead males stranded in the southern Iberian Peninsula (Bellido et al. 2015). It has been speculated that these male individuals were able to copulate with gravid females in the western Mediterranean, thus producing the subsequent nesting events, including those on Spanish beaches. Our results support an Atlantic parental (both male and female parents) origin of loggerhead nesting on the Spanish Mediterranean coast. Similar sporadic loggerhead nesting events have been recently observed in other sites from Mediterranean Sea (for example Delaugerre & Cesarini 2004, Bentivegna et al. 2008). Moreover, sporadic nesting events have been also observed recently for other sea turtle species. For example, until 2012, Peru was not considered a nesting site for sea turtles (Zavala & Kelez 2015); however, since 2012, Olive Ridley Lepi-

4 4 J. C. BÁEZ, D. MACÍAS, J. J. BELLIDO, J. A. CAMIÑAS dochelys olivacea and Green turtle Chelonia mydas have been regularly nesting there and in increasing numbers (Zavala & Kelez 2015). Given this background, we raise the issue of whether these sporadic nesting events could be a response to global warming or natural events. In this context, it is important to collect all the historical observations of nesting in the Mediterranean region to improve our knowledge of the historical reproductive behavior of loggerhead. On the other hand, it is necessary to apply recommendations regarding seasonal use of LLHB and conservation actions for adult loggerheads in the study area. Ack n o w l e d g e m e n t s. We are grateful to the Ministry of Environment and Spatial Planning of the Junta de Andalucía for providing data on strandings, and also to skippers and fishermen for providing data from the boats. 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