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Keywords:

  • Adaptive behaviour;
  • conservation management;
  • dispersal;
  • predictive models;
  • sample size;
  • spatial ecology;
  • telemetry

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information

Aim

Tracking the dispersal patterns and habitat use of migratory species is necessary to delineate optimal areas for protection, with large sample sizes being more representative of the population. Here, we examine the dispersal patterns of a key Mediterranean loggerhead turtle (Caretta caretta) breeding population to identify priority foraging sites for protection.

Location

Zakynthos Island, Greece and the wider Mediterranean.

Method

We examined the dispersal patterns and foraging sites of 75 adult loggerheads (n = 38 males and 37 females) tracked from the breeding area of Zakynthos Island (Greece) from 2004 to 2011. We then combined our data with published sea turtle literature to identify key foraging sites for protection.

Results

While both males and females exhibited similar dispersal patterns, about 25% males remained < 100 km of Zakynthos, whereas all females (except one) migrated > 200 km. Integration of our data with the wider literature isolated 10 core sites in proximity to existing protected areas, which could potentially protect 64% of the Zakynthos population, while five sites support individuals from at least 10 other loggerhead breeding populations.

Main conclusions

Due to the widespread availability of neritic foraging grounds across the Mediterranean, sea turtles from Zakynthos exhibit disparate dispersal patterns. However, protecting only a few objectively defined important sites can encompass a large proportion of the foraging areas used and hence have considerable conservation benefit.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information

Many animal populations invest in long-distance migration to reduce foraging competition when food resources are scarce at breeding sites (e.g. Greenwood, 1980; Alerstam et al., 2003; Fryxell et al., 2004). Hence, while a population may aggregate at one site to breed, many disparate foraging sites may be used depending on resource availability and the pattern of dispersal which may be influenced by factors such as wind direction, sea currents or land barriers in avian, marine and terrestrial migrants, respectively (e.g. Åkesson & Hedenstrom, 2007). Consequently, important habitats for protection may be distributed across wide regions, often traversing international borders or economic exclusion zones (e.g. Hannah et al., 2002; Bradshaw et al., 2010). At present, of the 150,000 protected areas across the world, just 3% are in the oceans (c. 5000 marine protected areas) (Bradshaw et al., 2010). Hence, as countries introduce measures to improve protection along their coastlines (Bradshaw et al., 2010), it is important to ensure that governments and environmental agencies select optimal sites for regulation (Ferrier, 2002).

Remote tracking systems of animals, using, for example, GPS or ARGOS, may generate extensive datasets that directly show the placement of individuals within ecosystems, portraying habitat use and migratory patterns. This technology provides an opportunity to collect fine-scale spatio-temporal information about species that would otherwise be difficult to study (i.e. tuna, Block et al., 2005; shearwaters, Shaffer et al., 2006; leopards, Gavashelishvili & Lukarevskiy, 2008). For instance, tracking studies of sea turtles, which are of world-wide conservation concern, have gained momentum over the last 20 years (Godley et al., 2008), with datasets of > 30 (max. 186) turtles from individual populations gradually emerging; however, these works are primarily focused on females and juveniles (e.g. Polovina et al., 2006; Hawkes et al., 2011), rather than males (but see Arendt et al., 2012a, b). In general, tracking studies of sea turtles have inferred (1) high fidelity of adults to foraging sites (e.g. Broderick et al., 2007; Schofield et al., 2010a), (2) seasonal variability in dispersal to foraging sites (e.g. van Dam et al., 2008; Hawkes et al., 2011; Zbinden et al., 2011), (3) male and female differences in dispersal and foraging site use (e.g. van Dam et al., 2008; Arendt et al., 2012a) and (4) phenotypic variation in foraging habitat (coastal versus oceanic) use within populations (e.g. Hatase et al., 2002, 2010; Hawkes et al., 2006). Several theories have been proposed to explain these differences, including (1) hatchling drift influenced by sea currents (Hays et al., 2010b; Gaspar et al., 2012), (2) the evolutionary context of food abundance predictability (Drakare et al., 2006; van Dam et al., 2008) and (3) possible adult mortality risk of migratory routes and foraging sites (van Dam et al., 2008).

The Mediterranean Sea has been the focus of extensive sea turtle research, including satellite tracking and by-catch studies (e.g. Broderick et al., 2007; Zbinden et al., 2008; Schofield et al., 2009; Casale et al., 2010; Schofield et al., 2010a; Zbinden et al., 2011). This work has resulted in the delineation of two Regional Management Units (RMU) for loggerhead sea turtles, representing populations from the Mediterranean and north-west Atlantic (Wallace et al., 2010), with green turtle (Chelonia mydas) populations also being resident to the region. Interestingly, while juvenile loggerheads from Atlantic populations enter the western Mediterranean basin (via the Strait of Gibraltar) for development (Casale et al., 2008; Eckert et al., 2008), the breeding and foraging habitats of permanent Mediterranean loggerhead and green populations are primarily concentrated in the central and eastern basins, with Zakynthos Island (Greece) in the central basin hosting the largest known breeding site for loggerhead turtles (Fig. 1a; Margaritoulis et al., 2003). Initial stranding data of dead turtles from Zakynthos (based on external flipper tag returns) that were washed ashore or entangled in nets indicated potentially broad dispersal to foraging sites (Margaritoulis et al., 2003); yet, this observation could have been an artefact of oceanic drift by dead or injured animals. However, subsequent satellite tracking studies began to support the stranding data, but indicated differences in movement patterns. For instance, a tracking study of 18 female loggerheads from Zakynthos (Zbinden et al., 2011) showed a clear dispersal pattern to foraging sites, either north (to the Adriatic) or south (to the Gulf of Gabes). In contrast, a tracking study of 10 males from the same site (Schofield et al., 2010a) showed primarily northerly dispersal to the Adriatic and Aegean. This raised the question of whether males and females use different foraging sites, or whether this was simply an artefact of sample size.

image

Figure 1. (a) The location of the breeding area of Zakynthos in the Mediterranean compared with other loggerhead (stars) and green (triangles) turtle nesting areas in the Mediterranean. The main seas of the Mediterranean that are cited in this study are indicated. (b) Migration of male (black, n = 31) and female (red n = 29) loggerhead turtles from the breeding area of Zakynthos in Greece to the primary foraging sites. Excluded tracks: five retracked (repeat tracked, either through the device operating for more than one year, or a new transmitter being attached) males; one male and five females without locations between the breeding and foraging sites. White star = Zakynthos. (c) Schematic showing the patterns (as actual numbers of turtles) of initial dispersal by male (n = 27) and female (n = 33) turtles on departing the breeding area (excluding residents, n = 5). Note: diagram not to scale.

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Hence, in this study, we assessed the dispersal and foraging destinations of 75 adult male and female loggerheads that were captured and tracked from the key Mediterranean breeding area of Zakynthos between 2004 and 2011. Based on our tracking data, we suggest where suitable neritic foraging habitat may lie in winter and summer months, enabling prioritization for conservation. Finally, we combine our data with published literature from other sea turtle (green and loggerhead) populations across the Mediterranean, to identify key foraging sites according to contributions of species, breeding population, sex and age class. This study supports the importance of using large datasets to correctly infer population level dispersal patterns and foraging habitat use, as well as to delineate important areas for the protection of sea turtles inhabiting the Mediterranean Sea.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information

Instrumentation

Between 2004 and 2011, 75 adult loggerhead turtles from Zakynthos, Greece, in the central Mediterranean basin (Fig. 1a; Table S1a, b; 37° 43′ N, 20° 52′ E), were instrumented with satellite transmitters (n = 38 males, of which five were tracked for more than one breeding season; n = 37 females, of which one was tracked for more than one breeding season). During May of 2007–2011, the Swansea University team attached 32 transmitters, and a further 25 transmitters were attached by the National Marine Park of Zakynthos (NMPZ) from 2008 to 2010 (combined total: n = 38 males; n = 19 females), when males and females aggregate to mate before the start of the nesting season. All turtles were captured at sea, within 1 km of shore, in the vicinity of the nesting beaches (for methodology see Schofield et al., 2010a). When possible, transmitters were retrieved one year after attachment, during in-water surveys or on the nesting beaches. Units provided either Global Positioning System (GPS) quality locations and/or Argos quality locations relayed either via the Argos satellite system or the mobile phone network. Table S1 lists the tracking devices used, with information on device programming, performance metrics and weights being available in our previous publications (e.g. Schofield et al., 2010a). The data were filtered using a maximum rate of travel of 5 km h−1 between successive locations (Luschi et al., 1998). Foraging sites were identified by individuals slowing down and remaining in fixed areas for extended periods of time (minimum of 5 days; see Hays et al., 2010a), using a combination of displacement distance and changes in speed of travel (Blumenthal et al., 2006; Schofield et al., 2010a). In addition, we digitized the previously published tracks of 18 female loggerhead turtles satellite tracked from 2004 to 2007 on the nesting beaches of Zakynthos (Zbinden et al., 2011), which are also listed in Table S1. This paper presents previously unpublished tracking information for 38 turtles (n = 22 males; n = 16 females).

All tracked turtles (males and females) were identified using a previously validated photo-identification system (Schofield et al., 2008) and external flipper tags (females only), with all turtles captured from 2008 onwards also receiving passive integrated transponders (PITs). From May 2009 onwards, following confirmation that males (Hays et al., 2010a), like females (see Broderick et al., 2007), return to their primary foraging sites, transmitters were only attached to previously untracked individuals, using the combined methods of identification. In the event of capturing previously tracked turtles, the individual was measured, photographed, identified, marked with paint (to avoid repeat captures in the same two-week period) and returned to the sea. Transmitters were not attached to turtles with signs of recent injury, large numbers of leeches, emaciation or flipper trauma/loss.

Dispersal

The direction of departure from Zakynthos was recorded for all turtles. The dispersal directions were grouped into five ‘regions’ of the Mediterranean Sea: (1) Region A, north, towards Amvrakikos and the Adriatic, (2) Region B, south-west, towards Tunisia (Gulf of Gabes) and Libya, (3) Region C, the vicinity of Zakynthos (the Ionian Sea), (4) Region D, to the Aegean Sea; and (5) Region E, to the western Mediterranean (Fig. 1a; Table 1). We compared the dispersal directions of the tracking datasets against published female stable isotope analyses from Zakynthos (Zbinden et al., 2011) and female strandings for Zakynthos (Margaritoulis et al., 2003) (Table 1). To avoid pseudoreplication in the analyses, for the six turtles tracked across two years, only data from the first year were used.

Table 1. Numbers of turtles tracked to foraging areas in each of the five regions in Fig. 1(a). Data are compared with the proportions of stranded loggerheads recorded in each region (Margaritoulis et al., 2003) and inferred foraging areas from stable isotope data (Zbinden et al., 2011)
RegionLocationTracking Strandings Females Stable isotope Females
Total MalesFemales
AAdriatic & Amvrakikos2810184522
BGulf of Gabes & Libya2110113025
CIonian (including residents)9 8130
DAegean633190
EWest Mediterranean11020
FOther00010
 Total65323310047

Foraging

The shortest (i.e. straight line) distance between the primary foraging sites and the breeding site was calculated. Foraging sites were classified as: (1) oceanic (> 200 m) (Seminoff et al., 2008), (2) neritic coastal (< 200 m seabed depth, < 2 km from shore) and (3) neritic open sea (< 200 m seabed depth, > 2 km from shore) (Schofield et al., 2010a). For the purposes of this study, discrete sites were given arbitrary numbers; however, they remain an artefact of sample size, whereby as sample size increases, so certain sites will merge. Here, we defined a foraging site as a single site or group of overlapping sites that are separated from adjacent sites by a minimum distance of 36 km, which reflects the mean migration speed (1.5 km h−1; SD ± 0.57; Schofield et al., 2010a) over a 24 h period, indicating directional movement. We recorded the location (latitude), mean depth (GEBCO, http://www.gebco.net/) and the category of all foraging sites (i.e. whether it was the first, second, etc. to be used after migrating from the breeding site) that were used by all turtles over the study period. Home ranges were not calculated, due to the different types of transmitters used, and differences in transmission frequency and accuracy. We used arcmap v9.1 (ERSI, Redlands, CA, USA; http://www.esri.com/software/arcview) to show the location of all foraging sites used by the tracked turtles across the Mediterranean. Where possible, we recorded the date that turtles shifted foraging sites and compared the frequency of movement according to geographical location and temperature. We also assessed the data for any differences in sex and body size [curved carapace length (CCL), from the nuchal scute to the tip of the longest supracaudal scute] with respect to migratory distances and the latitude of the foraging sites.

Following Hawkes et al. (2007), we modelled the potential available foraging habitat for loggerheads in the Mediterranean during summer (August) and winter (February). We used a maximum seabed depth of 100 m (as 60 of 61 turtles foraged at sites shallower than 100 m depth) and a minimum temperature of 13 °C, based on minimum Mediterranean wintering temperatures recorded by Hochscheid et al. (2007), and the fact that no turtles in this study inhabited waters below this temperature. Bathymetric data were derived from GEBCO. Sea surface temperature (SST) data were derived from MODIS (Moderate Resolution Imaging Spectrometer) satellite data products (http://oceancolor.gsfc.nasa.gov/). We used the mean February SST from 2000 to 2010. These freely available gridded data products were resampled to the UTM map projection to facilitate the measurement of habitat area under SST and depth constraints. The general foraging ground locations of all turtles (except one) in each season clearly fell within the model parameters for each season; therefore, it was not necessary to further validate the model using filtered satellite location data (as performed by Hawkes et al., 2011) and was not possible here due to the use of different tracking units, with different quantities of locations at very different resolutions.

Protection

We evaluated the relative importance of the identified foraging sites based on available published data, with the aim to guide managers regarding the sites requiring immediate protection focus. As the Mediterranean is an almost enclosed sea that hosts around 24 known sea turtle (loggerhead and green) nesting areas across around 16 countries (Margaritoulis et al., 2003), we assimilated published literature on adult sea turtles for this region (see Table S2) that provided evidence for the presence of foraging sites, in addition to the use of known adult foraging sites by juvenile turtles. Data were assimilated from tracking, genetic, capture-recapture, tagging, by-catch and stranding studies. We then arranged the foraging sites according to species (green/loggerhead), sex (male/female), size class (adult/juvenile), number of represented breeding populations, seasonality of site (i.e. summer, winter or year-round use) and existing protection status of the site. Finally, we considered the likelihood of these sites receiving protection based on local, national and regional status in relation to the breeding area.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information

Turtles

The mean CCL of male loggerheads was 82.9 cm (n = 33, SD ± 7, range: 71–102 cm), while that of females was 83.7 cm (n = 35, SD ± 4.5, range: 74–91 cm). Four transmitters stopped working when turtles were still within the breeding area and were excluded from the dataset, leaving 32 males and 33 females for the dispersal analysis. Of the remaining transmitters, four stopped working during the post-breeding migration, which were excluded from the foraging site analyses, leaving 29 males and 32 females.

Dispersal

In general, males and females exhibited similar dispersal patterns from Zakynthos, with 70% travelling south-west and 30% travelling south-east (Fig. 1b, c). Most turtles migrated either north to the Adriatic Sea and Amvrakikos Gulf (Region A, 42%) or south-west to Libya and Tunisia (Region B, 32%), with the remainder staying in the Ionian Sea (Region C) or migrating to less frequented areas in the east (Region D) and west (Region E) Mediterranean. Significantly more males than females remained within 100 km of Zakynthos (G test, P < 0.001; 24% and 3%, respectively). This difference in use of the Ionian Sea between males and females was reflected in the comparison of the proportion of turtles in each of the five regions for the male and female tracking (n = 65), female stable isotope (n = 47; Zbinden et al., 2011) and female stranding (n = 100; Margaritoulis et al., 2003) datasets. The correlation coefficient of male tracking data with the female stranding data was much lower (0.72) than the female tracking data with the female stranding data (0.97) or the stable isotope data (0.87).

Foraging

After breeding, all turtles migrated to neritic sites shallower than 100 m, except one male that travelled directly to an oceanic site. In total, six turtles (male n = 4; female n = 2) frequented both neritic and oceanic sites during the tracking period. Foraging sites were widely dispersed across the three basins (Fig. 2a; Table S2; see Supporting information for detailed description); however, sites used by 65% of turtles were primarily concentrated in the north and south parts of the central basin, supporting the habitat model indicating that the central basin has the greatest percentage of available foraging habitat of < 100 m seabed depth (Fig. 2b; Table 2). Several turtles (n = 11 males; n = 12 females) used up to four separate sites, most of which frequented primary sites at 40–45°N latitude (n = 16 northern sites versus n = 7 southern sites) and moved south to latitudes < 40°N where the temperature remained above 13 °C year-round (Fig. 2c; Table 2).

Table 2. Potential available neritic foraging habitat in the western, central and eastern Mediterranean at a maximum seabed depth of 100 m (as all neritic study sites were within 100 m depth, except one) and showing the reduction in habitat availability during winter (based on minimum Mediterranean wintering temperatures of 13 °C determined by Hochscheid et al., 2007). Bathymetric data were derived from GEBCO. Sea surface temperature (SST) data were derived from Moderate Resolution Imaging Spectrometer (MODIS) satellite data products (http://oceancolor.gsfc.nasa.gov/)
BasinTotal area (km2)% Total area < 100 m seabed depth% Total area < 100 m seabed depth with February SST > 13 °C
West831,3006.83.5
Central861,20016.49.5
East765,4007.74.5
Total2,457,90010.55.9
image

Figure 2. (a) Discrete foraging sites frequented by male (black triangles) and female (grey triangles) loggerheads from Zakynthos (with some turtles frequenting more than one site). The foraging sites are indicated and numbered; orange numbers = foraging sites overlapping or in close proximity to existing marine protected areas and/or national parks. Discrete foraging sites are arbitrary and defined as a single site or group of overlapping sites that are separated from adjacent sites by a minimum distance of 36 km, which reflects the mean migration speed of loggerhead turtles (1.5 km h−1; Schofield et al., 2010a, b) over a 24 h period. In addition, other known loggerhead (filled dark grey circles) and green turtle (filled grey circles) foraging sites are shown based on the published literature (Bentivegna, 2002; Margaritoulis et al., 2003; Broderick et al., 2007; Hochscheid et al., 2007; Casale et al., 2008). Note: solely juvenile foraging sites of the West Mediterranean have not been included here. (b) Available foraging habitat for loggerheads in the Mediterranean to 100 m seabed depth (yellow contour) and 200 m seabed depth (blue contour) derived from GEBCO. For percentages, please see Table 2. (c) Sea surface temperature data delineating the 13 °C minimum temperature limit (pink contour) in February from 2000 to 2010 using MODIS. For percentage of 100 m seabed depth lost to loggerheads in winter, please see Table 2.

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Excluding residents to Zakynthos island (n = 5), foraging sites were on average 777 ± 334 km (range 50–1537) distant from the breeding site. Migratory distance was not correlated with CCL (F1,60 = 2.6, r2 = 0.05; P = 0.1). Furthermore, there was no difference in the mean (and SD) CCL between neritic versus oceanic foragers (mean 84 ± 2 vs. 82 ± 8 cm CCL, respectively); however, the sample size of the latter group was small (n = 6), with five individuals investing in both oceanic and neritic foraging. In addition, we found that the latitude of the primary foraging site was associated with CCL, with possible longitudinal variation in CCL too (see the supplementary information and Fig. S1 for more details.)

Protection

Figure 2a shows that about one-third of identified foraging sites (n = 10) used by the Zakynthos population are near to (< 20 km; n = 3 sites) or directly overlapping (n = 7 sites) existing MPAs and/or national parks (Abdulla et al., 2008; Table 3; Table S2). If the protection area and associated measures were extended to these 10 locations, 64% of turtles (62% males and 64% females) from Zakynthos could potentially be protected, at least for part of the year, with limited additional management effort. Unfortunately, half of these sites are only used during the summer by turtles, with wintering sites at unprotected locations. The improvement of protection measures at three existing protected areas in Greece (Sites 16, 19 and 20, all in the Ionian Sea) could safeguard 20% of turtles (28% males and 12% females) from Zakynthos, in addition to adult turtles from other breeding populations and juvenile green and loggerhead populations (Table 3; Table S2). At a regional scale, there are two focal areas for foraging site protection, the Gulf of Gabes and the Adriatic. In the Adriatic, the establishment of protection measures at Site 25 could safeguard 18% of turtles (20% males and 16% females) from Zakynthos; however, this site was only used by turtles during the winter months, although turtles from other adult breeding populations, as well as juvenile loggerheads (and possibly greens), have been documented in this area (Table 3; Table S2). In comparison, the protection of Sites 4 and 5 in the Gulf of Gabes could safeguard 31% (30% males and 34% females) of turtles throughout the year, with loggerhead turtles from up to 10 other breeding populations, as well as juvenile loggerheads, also frequenting these two sites (Table 3; Table S2).

Table 3. Summary table of the focal foraging sites of Zakynthos (Greece) loggerheads in the Mediterranean, and potential overlap with other breeding and juvenile populations based on evidence from the published literature (satellite tracking, live and dead strandings, mark–recapture, by-catch, genetic analyses). See Table S2 for full listing and associated references and Fig 2a. for foraging site locations. Site is the foraging site number listed in Fig. 2a. Breeding no. is the number of loggerhead breeding areas represented at each foraging site frequented by Zakynthos turtles
SiteBasinCountryForaging categoryThermal availabilityProtection in vicinityRecorded speciesGender/age class Loggerhead breeding populationsSources
LoggerheadGreenNo.Location
  1. Foraging category, NO, neritic open sea; NC, neritic coastal. Recorded species, Log, loggerhead; Gre, Green; Gender/age class, M, adult male; F, adult female; Juv, juveniles, with gender not differentiated. Breeding populations, ?, unconfirmed; Zak, Zakynthos, Greece; Kyp, Kyparissia, Greece; Cyp, Cyprus; Syr, Syria; T, Turkey; Mess, Messina; Lib, Libya; Tunis, Tunisia; Cal, Calabria; Is, Israel; It, Italy. Sources, 1, this paper; 2, Bentivegna (2002); 3, Margaritoulis et al. (2003); 4, Broderick et al. (2007); 5, Casale et al. (2007); 6, Hochscheid et al. (2007); 7, Echwikhi et al. (2010); 8, Chaeib et al., (2012); 9, Casale et al. (2013, 2012); 10, Rees et al. (2013); 11, Lazar et al. (2004a, b); 12, Casale et al. 2013, 2012; 13, Saied et al., 2012.

4CentralTunisiaNC/NOYear-roundNoLog M/F/Juvn/a~11Zak; Kyp; Cyp; Turk; Mess, Lib; Tunis; ? Cal,?Is,?It

1, 2, 3, 4, 5

6, 7, 8, 9, 12

5CentralTunisiaNC/NOYear-roundNoLog M/F /Juvn/a~6

Zak; Kyp; Cyp; Turk;

Tunis; Lib

1, 2, 3, 4,

5, 6, 7, 13

16CentralGreeceNCYear-roundYesLogM n/a 1Zak1
20CentralGreeceNCYear-roundYesLog/GreM/F /JuvJuv~4Zak; Syr; ?Kyp, Unknown1, 2, 3,5, 10
25CentralCroatiaNOSeasonal (summer)YesLogM/F/Juvn/a~2Zak; Kyp1, 5, 11

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information

The present study shows that turtles from a key loggerhead sea turtle population in the Mediterranean exhibit variable dispersal patterns, due to the large availability of neritic foraging habitat throughout the region. As we tracked over 30 males and 30 females in the current study, the observed dispersal patterns are considered to be representative for this population, allowing any differences between the sexes to be clearly defined. However, while the sample size of the current study is large compared with the majority of existing sea turtle studies (see Godley et al., 2008), the tracked individuals in this study still only represented about 9% of this breeding population (Schofield et al., 2010b). Hence, it was necessary to draw on available tracking, stranding and genetic information from the wider literature to delineate core foraging areas for protection.

It is possible that we may have missed foraging areas that are rarely used by the Zakynthos adult breeding population, despite the size of the tracking dataset. For instance, adult turtles foraging in the Bay of Naples have been tracked to foraging and breeding sites in the central Mediterranean (Bentivegna, 2002; Hochscheid et al., 2007). Furthermore, increased tracking is revealing increased behavioural plasticity (e.g. Hatase et al., 2007; Seminoff et al., 2008; Rees et al., 2010; Schofield et al., 2010a), which confers some resilience against change, despite complicating the identification of all core foraging areas.

Interestingly, while our previous work using n = 10 males (Schofield et al., 2010a) indicated a bias of male movement towards northerly foraging sites, once the sample size exceeded 20 individuals, similar numbers dispersed north as south, more closely reflecting that observed for females from the same population. Furthermore, the current study supported adult female tag returns from the stranding datasets (Margaritoulis et al., 2003), as well as hatchling drift scenarios (Hays et al., 2010b). However, this consistency across studies was stronger for tracked females compared with tracked males. Male dispersal deviated from that of females in that 24% of males remained resident or close (< 100 km) to the breeding area, supporting recently published studies (Shaver et al., 2005; van Dam et al., 2008; Arendt et al., 2012a). Yet, studies on Cyprus (loggerheads, Broderick et al., 2007) and the Galapagos (green turtles, Seminoff et al., 2008) have recorded females resident to the general area; hence, we may have just not yet tracked a resident female. The observed difference in migratory pattern between the sexes at Zakynthos, and other areas, may be due to males facing much lower reproductive costs/investment compared with females (Clutton-Brock & Vincent, 1991). Similar differences in movement patterns and habitat use between the sexes have also been recorded for other species (e.g. wandering albatrosses, Weimerskirch et al., 1997; fur seals, Boyd et al., 1998). This behaviour might facilitate more opportunistic foraging strategies by males, as well as allow annual reproductive activity and greater (earlier) access to returning females (for review see Morbey & Ydenberg, 2008).

In contrast to Hatase et al. (2010) in the Pacific, but similar to Hawkes et al. (2011) in the Atlantic, the majority of male and female loggerheads frequented neritic foraging sites of < 100 m seabed depth in the central Mediterranean, either to the north (Adriatic) or south (Gulf of Gabes), with only a few individuals using oceanic sites. This north versus south division is similar to that recorded by Hawkes et al. (2011) in the Atlantic. Furthermore, our habitat model showed that these two areas of the Mediterranean support the greatest areas of available foraging habitat in the Mediterranean. Due to sea temperatures dropping below 13 °C in winter (i.e. the minimum Mediterranean wintering temperatures recorded by Hochscheid et al., 2007) in the northern area, turtles were more likely to use more than one foraging/wintering site and move southward compared with those inhabiting the southern area.

High neritic habitat availability, multi foraging site use and temperature regulated shifts to wintering sites make establishing focal areas for protection in the Mediterranean extremely challenging. Despite this, tracking datasets from the current study combined with existing publications, based on tracking and other techniques (i.e. stranding, capture-recapture and genetics), produced baseline information identifying key foraging sites for protection at national and regional levels. At a regional scale, pressure to protect the Zakynthos population is extremely difficult due to the complexity of national boundaries and competition between governments and government agencies regarding jurisdictional responsibility (Agardy, 1994). Furthermore, detailed by-catch studies, from the Adriatic to the Gulf of Gabes (Casale et al., 2008, 2010; Echwikhi et al., 2010; Chaieb et al., 2012), clearly indicate the high risk of mortality to sea turtles as a result of intensive fisheries activities in these key foraging sites. However, in both regions, we identified key areas for protection that would also safeguard adult and juvenile turtles from at least 10 other breeding sites. At northern sites, which are primarily used by turtles in the summer, seasonal protection measures could be introduced, with different levels of fisheries activity being permitted in different seasons (Hannah et al., 2002). At a national scale, within the Ionian Sea of Greece, we reaffirm the need to establish a large multiple use protected area, with an integrated coordinated management system providing varying levels of protection. Within this framework of small MPAs (López Ornat, 2006), six foraging and/or breeding sites (including Zakynthos) would receive protection, which are frequented by year-round resident males, sexually active males shuttling between breeding sites (Schofield et al., 2010a, b) and reproductive females conducting forays among sites (Schofield et al., 2010a, b). Furthermore, we recommend that protective legislation and effective management should be strengthened in Amvrakikos Gulf, as the existing national park primarily focuses its protection actions in the northern section (transitional ecosystems/wetlands) of the marine area (see also Rees et al., 2013). To further refine important areas for conservation planning, it is important to assimilate all available environmental criteria (e.g. Edwards & Richardson, 2004; Coll et al., 2010), including areas of seasonal use and how the distribution of sea turtle foraging sites might change over time (Hannah et al., 2002; Araújo et al., 2004).

In conclusion, our study provides a good example of a sea turtle population with high variability in dispersal and foraging habitat use, demonstrating the importance of having large tracking sample sizes to infer core areas for protection at an ocean basin scale.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information

The authors thank the National Marine Park of Zakynthos (NMPZ) for the permission to conduct this research, and the sponsors of the Management Agent's termed Caretta's Odyssey which spanned 2008 to 2010 for 25 transmitters. The 32 Swansea University transmitters were financed by the AXA Research Fund, Boyd Lyon Sea Turtle Fund, British Chelonia Group, People's Trust for Endangered Species, Project Aware, Swansea University and Thermadap. We thank Suzanne Bevan, who pre-processed the MODIS SST product. We thank the many people who provided in-water capture assistance, including the NMPZ coast guards. We acknowledge use of the Maptool program (http://www.seaturtle.org).

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  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information
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Biosketch

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information

Gail Schofield is a behavioural ecologist, whose work focuses on applying scientific research to conservation practice using direct and indirect techniques, such as satellite telemetry and videography. Her work has investigated the effects of various parameters effect both small and large scale movement patterns of vertebrates, including breeding, foraging and migration ecology. This work constituted a major collaborative effort combining data assimilated by GS and colleagues at Swansea University with the National Marine Park of Zakynthos Management Agency (http://www.nmp-zak.org/). Further information about GS and publications can be found at http://scholar.google.gr/citations?user=JuAIkOoAAAAJ&hl=en and http://www.swan.ac.uk/bs/turtle/hays_publications2.htm.

Author contributions: G.S., S.F. and G.C.H. conceived the study; A.D.K. obtained the funding for the 25 NMPZ transmitters; G.C.H., G.S. and S.F. obtained the funding for the 32 Swansea University transmitters; G.S., S.F. and M.K.S.L. conducted the fieldwork attaching all 57 transmitters; G.S., K.A.K. and A.D. compiled the data; G.S. and G.C.H. led the data analyses and interpretation with contributions from all authors; A.L. conducted the GIS analysis; G.S. wrote the paper with contributions from all authors.

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Biosketch
  10. Supporting Information
FilenameFormatSizeDescription
ddi12077-sup-0001-FigS1-TableS1-S2.docxWord document186K

Figure S1 Variation in sea turtle body size (CCL) with latitude of foraging area (F1,60 = 15.05, r2 = 0.2; P < 0.001).c

Table S1 Deployment details for the 75 tracked turtles: (a) male (n = 38, of which five were tracked for more than one breeding season) and (b) female (n = 37, of which one was tracked for more than one breeding season).

Table S2a. Summary information of the foraging sites identified across the Mediterranean using adult male and female loggerheads tracked from Zakynthos, Greece. S2b. Published literature used to identify overlap in foraging sites with Zakynthos turtles (A) based on tracking datasets and (B) based on genetic data.

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