Distribution and temporal trends in the abundance of nesting sea turtles in the Red SeaBiological Conservation 261 (2021) 109235
Available online 3 August 2021 0006-3207/© 2021 Elsevier Ltd. All rights reserved.
Distribution and temporal trends in the abundance of nesting sea turtles in the Red Sea
Takahiro Shimada a,b,c,d,*, Mark G. Meekan a, Robert Baldwin e, Abdulaziz M. Al-Suwailem f, Christopher Clarke f, August S. Santillan f, Carlos M. Duarte b
a Australian Institute of Marine Science, Crawley, Western Australia 6009, Australia b Red Sea Research Center and Computational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia c UWA Oceans Institute and School of Biological Sciences, University of Western Australia, Crawley, WA, Australia d Department of Environment and Science, Queensland Government, GPO Box 2454, Dutton Park, QLD 4001, Australia e Five Oceans (Environmental Services) LLC, Box 660, PC 131, Oman f Beacon Development Company, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
A R T I C L E I N F O
Keywords: Population ecology Coastal development Climate change Red Sea Nesting seasonality Sea turtle
A B S T R A C T
Mobile species often aggregate at predictable places and times to ensure that individuals find mates and breed in suitable habitats. Sea turtles demonstrate this life history trait, which can make these species highly susceptible to population declines if nesting habitats are lost or degraded. Conservation management thus requires knowl- edge of where and when turtles nest and changes in abundance in these habitats through time. Here, we compiled new and published data and used a novel analysis to describe seasonality, annual abundance and spatial distribution of nesting green (Chelonia mydas) and hawksbill (Eretmochelys imbricata) turtles in data- deficient populations that inhabit the Red Sea. Major new rookeries were identified for green turtles at Jazirat1 Mashabah (113 and 179 nesting females in 2018 and 2019) and for hawksbill turtles at Jazirat Al Waqqadi (79 nesting females in 2018), both of which are located on nearshore islands of the Kingdom of Saudi Arabia in an area subject to industrial, residential and ecotourism developments. An upward trend in annual abundance of nesting sea turtles was estimated at some sites including Ras Al Baridi (Saudi Arabia), a major rookery of green turtles in the Red Sea, where the annual numbers increased from 14–110 individuals in 1982–1995 to 178 and 330 individuals in 2018 and 2019. This integrative work provides the most up-to-date, comprehensive information on nesting sea turtles in the Red Sea and documents a critical baseline for sea tur- tle conservation and future management effort.
1. Introduction
Mobile species, such as birds, fishes, large mammals and reptiles often aggregate predictably in the same place and time for breeding over years and generations (Baker et al., 2013; Groot and Margolis, 1991; Miller, 1997; Wheelwright and Mauck, 1998). This spatio-temporal fi- delity to particular breeding sites ensures that individuals, which might otherwise be widely distributed for foraging across an environment, can find mates and reproduce in suitable habitats (e.g. Shimada et al., 2020). However, the loss or degradation of these habitats can have significant repercussions for the viability of populations, which is a situation faced by many species today, due to anthropogenic threats such as
development, pollution and climate change (Cristofari et al., 2018; Venter et al., 2016).
Sea turtles provide good examples of such species. These animals aggregate to breed at certain places and times across generations, and strong fidelity to breeding habitats has resulted in distinct genetic stocks within the species range (Jensen et al., 2013; Miller, 1997). Nesting is focused on sandy beaches where females deposit eggs. Anthropogenic threats in nesting beaches include loss or modification of suitable nest- ing beaches, light pollution due to industrial or residential de- velopments, and climate change driven extreme storm surges, sea level rise and warming (Fuentes et al., 2010; Laloe et al., 2017; Pendoley and Kamrowski, 2016). Combined with incidental boat strikes, by-catch in
* Corresponding author at: Department of Environment and Science, Queensland Government, GPO Box 2454, Dutton Park, QLD 4001, Australia. E-mail address: taka.shimada@des.qld.gov.au (T. Shimada).
1 ‘Jazirat’ is the Arabic word for ‘island of’.
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fisheries, targeted hunting of adults, harvesting of eggs, and predation on hatchlings and adult females by feral animals (Campbell, 2003; Gronwald et al., 2019; Shimada et al., 2017), these threats have resulted in the long-term decline of major sea turtle populations throughout species ranges. Although some populations of sea turtles have shown signs of recovery (Chaloupka et al., 2008; Mazaris et al., 2017), today, many species are still categorised as Endangered or Critically Endan- gered by the International Union for the Conservation of Nature Red List (IUCN, 2020).
The spatial concentration of nesting sea turtles, and the vulnerability of adults, eggs, and hatchlings during this phase offers an obvious focal point for cost-effective conservation and management strategies that seek to halt or reverse ongoing declines in populations (Hamann et al., 2010). Of particular concern are those stocks that are poorly docu- mented and/or facing imminent potential threats from developments driven by growing populations of humans in coastal environments. The Red Sea contains populations of the Vulnerable green (Chelonia mydas) and Critically Endangered hawksbill (Eretmochelys imbricata) turtles (IUCN, 2020; Mancini et al., 2019) that are thought to be genetically distinct from others in the wider Indian Ocean (Jensen et al., 2019). At
present, we lack any estimates of recent and long-term patterns in abundance that might be used to determine trajectories of these pop- ulations (Wallace et al., 2010). Additionally, turtles in the Red Sea breed on islands and coastlines that are now undergoing rapid change through very large developments, most notably three projects in the Kingdom of Saudi Arabia (Saudi Arabia hereafter) that encompass many dozens of nearshore islands and hundreds of kilometres of the mainland coast (PIF, 2017). For these reasons, there is an urgent need for data on breeding patterns to support appropriate conservation strategies for sea turtles in the region.
Our study aimed to address this issue by reporting the outcome of large scale (several hundreds of kilometres) surveys of nesting sea turtles along the coastlines and islands of the north-eastern Red Sea conducted since 2018. To provide a comprehensive review of sea turtle nesting in the Red Sea, we consolidated this new data and published information on seasonality, distribution and abundance in nesting patterns. We also examined trends in abundance of nesting green and hawksbill turtles at some locations where repeated surveys had been conducted. This work provides a revised baseline for sea turtle conservation in the region and contributes to global assessments of sea turtle population status such as
Fig. 1. Study sites across the north-east Red Sea. Each symbol is a beach with evidence of nesting by green turtles (green circle), hawksbill turtles (purple triangle), or both green and hawksbill turtles (orange square). Beaches that were surveyed but no evidence of nesting was found are shown by black points. Grey polylines show the marine boundaries of three development projects (NEOM, Amaala, TRSP) and the general area of Ras Al Baridi. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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2.1. New data
2.1.1. Study area and dataset Field work was conducted between 2018 and 2020 along the Saudi
Arabian coast of the north-eastern Red Sea, where little prior informa- tion on use by sea turtles was available (Supplementary Material – Sections A and B). Location and timing of surveys was dictated by lo- gistics, resulting in unequal coverage and survey effort across time and space (Supplementary Material – Section A). Our surveys included Ras Al Baridi (a known major rookery of green turtles in the Red Sea) in Al Madinat al Munawwarahas province as well as islands and coastal areas designated for industrial, residential and ecotourism development in Tabuk province (Fig. 1). The latter are officially named as NEOM, Amaala and The Red Sea Project (TRSP) from north to south (PIF, 2017). In 2018, we surveyed all potential nesting beaches of 49 islands and extensive lengths of the mainland coast (>500 km) over 24 days be- tween February and August. In 2019, we revisited three islands (An Numan, Mashabah, Al Waqqadi) and mainland beaches at Amaala and Ras Al Baridi over 15 days between June and December. In 2020, three islands (An Numan, Shaybarah, Al Waqqadi) and Ras Al Baridi were surveyed over 5 days between January and March. Details of site and timing of each survey are described in Supplementary Material – Sec- tions A and B.
At each site we recorded the nests and tracks of turtles on beaches. Entry to and exit from a beach were recorded as a single track. We closely examined nests and tracks to identify the outcome of nesting activity based on signs such as the presence or absence of egg chambers, the shapes of body pits, and nest camouflaging. A nest with evidence of egg deposition was categorised as a clutch, whereas a nest and a track without a clear evidence of egg deposition was categorised as an emergence. The age of each clutch and emergence was also estimated as ≤1 day, ≤2 weeks, ≤1 month, >1 month old, or last season. The age categories within a breeding season were assigned by observation of physical evidence including debris, footprints, crab mounds, tidal wash and vegetation. As very little rain falls between spring and autumn (nesting season) at our study area (<5 mm in total; Mashat and Abdel Basset, 2011), we assumed few tracks were eroded by rain during a nesting season. However we assumed that tracks were eroded during a wet season, which occurs between breeding seasons (Mashat and Abdel Basset, 2011). This assumption was validated by the observation of several marked tracks across a nesting season. More details of how we examined and aged each nest and track are provided in Supplementary Material – Section C.
2.1.2. Detection of nesting season The seasonal trend of nesting activities (nesting seasonality) was
examined based on the dates of our surveys and estimated age of each clutch and emergence. Due to the large latitudinal differences and un- balanced frequency of surveys and timing among sites, we grouped the data into two regions (NEOM – Amaala and TRSP – Ras Al Baridi) and determined seasonality per region and species (Fig. 1). The date of each clutch and emergence was calculated by subtracting half of the esti- mated age from the date of the survey as the most parsimonious rule. For example, if a ≤1 month old emergence was recorded on 16 August, it was associated with 1 August (16 minus 30/2 days). For this analysis, we only used the clutches and emergences that were estimated to be ≤1 month old, so that estimated dates could be assigned to each record without prior knowledge of nesting seasonality (i.e. start and end of nesting season). End of nesting season was further confirmed by satellite tracking data collected from 30 green turtles that nested at Jazirat Mashabah and Ras Al Baridi in 2019 (Shimada et al., 2021). Collectively, the NEOM – Amaala region was surveyed at least once per month for 8
months between July and February except for September. The TRSP – Ras Al Baridi region was surveyed at least once each month for a year. The peaks of the nesting seasons were only identified at sites where more than one survey was conducted within the respective nesting season (Supplementary Material – Section D).
2.1.3. Abundance of nesting turtles At most sites, our surveys likely captured the representative number
of clutches and emergences that occurred up to the last survey. For this analysis, we used all the clutches and emergences that were estimated to have occurred within the respective nesting seasons. The cumulative number of clutches (Clutchesk) laid by a species up to the last survey date was calculated as:
Clutchesk = ∑k
i=1 (Clutchesi +Emergencesi⋅NS) (1)
where k was the number of surveys conducted at a site in the year, Clutchesi and Emergencesi were the number of clutches and emergences recorded at the ith survey, and NS was the nesting success rate (proba- bility of egg laying per emergence). The mean NS rate in this region was estimated to be 0.628 in the satellite tracking study of 20 green turtles that nested at Jazirat Mashabah (n = 13) and Ras Al Baridi (n = 7) during the 2019 nesting season (Shimada et al., 2021). This constant NS rate was used in Eq. (1) across the sites because the NS rate did not differ between Jazirat Mashabah and Ras Al Baridi despite the contrasting environmental settings; Jazirat Mashabah is uninhabited whilst at Ras Al Baridi anthropogenic impacts are possibly greatest among all north- eastern Red Sea rookeries (Pilcher, 1999; Shimada et al., 2021; this study). The rates of NS calculated for green turtles were also applied to emergences of hawksbill turtles as the mean NS rates of both species are very similar when they nest on the same beaches (Kameda and Wakat- suki, 2011 and Sea Turtle Association of Japan, unpublished; Mortimer et al., 2011; Okuyama et al., 2020).
If the total number of clutches (Clutches) and individual’s clutch frequency per nesting season (Clutch frequency) are known, the annual abundance of nesting turtles (Turtles) at a site can be calculated as:
Turtles = Clutches
Clutchfrequency (2)
This simple method could only be applied to 13% of our data, which likely represent the annual total of clutches and emergences at the respective nesting sites. This small portion of the data was collected during the last half of the nesting season at the sites where nests and tracks remained visible for several months (Supplementary Material – Section C). The remaining data (87%) represent the partial count of clutches and emergences in the respective seasons because the surveys were conducted only up to the middle of the nesting season, and thus the subsequent clutches and emergences that might have occurred within the same nesting season were not recorded.
It is possible to estimate the annual abundance of clutches from partial count data if the proportion of the collected data relative to the total annual abundance is known. For a breeding population that only has one cohort per nesting season, this estimation can be relatively simple. For example, at Bramble Cay in Australia (Limpus et al., 2001), the number of available nesting green turtles since the beginning of a nesting season (Days), calculated as the number of turtles that arrived at the nesting ground minus those departed, closely follows a normal dis- tribution with the mean (μ) and standard deviation (σ) of Days (Sup- plementary Material – Section E), and so can be modelled as:
Days ∼ N ( μ, σ2) (3)
This means the expected proportion (Proportionk) of the clutch number up to the last day of survey (Dayk) relative to the total annual number can be calculated from the cumulative density function of a normal distribution as:
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Dayfirst f (x)dx, for Dayk ≤ Daylast (4)
where Dayfirst and Daylast are the first and last days of a nesting season at a given site for the species and when Dayk > Daylast, Daylast was replaced with Dayk. We verified that the annual total clutches and emergences known (13% of our data) followed the cumulative distribution functions of the normal distribution (Fig. 2). For each region (NEOM – Amaala, TRSP – Ras Al Baridi) and species (green, hawksbill), the mean for the normal distribution was the mid-point of the estimated nesting season because, similar to the example of the Bramble Cay green turtles, there was only one nesting season cohort for each species at our sites (Sup- plementary Material – Section D). Standard deviations and 95% confi- dence intervals (CI) were estimated from the data by maximum likelihood estimation using the R packages stats and stats4 (R Core Team, 2020). We used those probability density functions, prepared for each region (NEOM – Amaala, TRSP – Ras Al Baridi) and species (green, hawksbill), to calculate the expected proportion (Proportionk) of the cumulative number of clutches (Clutchesk) up to Dayk relative to the total annual abundance. The annual clutch numbers (Clutches) of a species at each site and nesting season was then:
Clutches = Clutchesk Proportionk
(5)
Finally, we estimated the annual abundance of nesting turtles (Tur- tles) per site and species by including the estimated annual clutch numbers (Clutches) in Eq. (2). For Clutch frequency in Eq. (2), we used the global means, which are 5.9 clutches for green and 2.74 clutches for hawksbill turtles (Esteban et al., 2017; Miller, 1997). These values are likely to be accurate approximations of the true mean clutch frequencies of the nesting turtles in this region (Pilcher et al., 2014; Shimada et al., 2021).
We applied the above procedure to most datasets where all the clutches and emergences up to the last survey dates were presumed to be collected (Supplementary Material – Section C). Exceptions were the data collected only once during a nesting season of green turtles at Ras Al Baridi in 2018, and at two islands (Mashabah, Al Waqqadi) in 2019. At these sites most tracks only remain apparent for no more than a month because of the high density of nesting, and in the case of Ras Al Baridi, a large amount of wind-blown cement dust from a nearby factory that accumulates over the nesting beaches (Pilcher, 1999; Supplemen- tary Material – Section C). As these surveys only captured snapshots of clutches and emergences, the estimation method described above was not applicable. Instead, we contrasted the number of emergences of these snapshot data to those of frequent surveys at Ras Al Baridi in 2019 (Supplementary Material – Section A). In 2018 at Ras Al Baridi, the survey was conducted on 20 August (Emergences20Aug2018) and the same beaches were surveyed again on 21 August in 2019 (Emergence- s21Aug2019). The annual abundance of green turtles that nested at Ras Al Baridi in 2018 (CMRB2018) was estimated proportionally from the annual abundance estimated for 2019 (CMRB2019) as:
CMRB2018 = Emergences20Aug2018 Emergences21Aug2019
⋅CMRB2019 (6)
Similarly, the single surveys conducted at two islands (Al Waqqadi, Mashabah on 7, 8 September 2019 receptively) were contrasted with the data collected at Ras Al Baridi on 4 September 2019 to proportionally estimate the annual abundances from CMRB2019.
2.2. Published information
We examined literature cited by seminal reviews and reports (Man- cini et al., 2015; Phillott and Rees, 2019) and 524 papers published after 2015 as identified by a Google Scholar search (14 March 2021) using a combination of key words “Red Sea”, “nesting”, and “turtle”.
Due to variation in the technique and timing of data collection in the literature, we standardised historical estimates of the annual abundance of nesting female turtles using the above procedures (2.1.3). We fine- tuned estimates case by case, based on timing and duration of each survey and the nesting seasonality of the species at each site. Details of historical data, each adjustment, and standardised estimates are pro- vided in Supplementary Material – Section F.
Where estimates were available for more than one season, annual abundance was averaged over the three most recent years of surveys. Worldwide, individual female green and hawksbill turtles breed on average once every three years (Miller, 1997).
2.3. Abundance trend of nesting turtles
To compare trends among sites and years, data were standardised to estimate annual abundance of nesting turtles as described above and in Supplementary Material – Section F.
3. Results
Between 2018 and 2020, we recorded a total of 4613 and 1329 clutches and emergences of green and hawksbill turtles respectively along the Saudi Arabian coast of the northern Red Sea (Supplementary Material – Section F). Among these we identified 3158 green and 713 hawksbill clutches and emergences that had occurred within the respective nesting seasons, and these were used to estimate the annual abundance of nesting females at each site. This new evidence of nesting was collected at 26 sites (23 island and 3 mainland) for green turtles and 50 sites (46 island and 4 mainland) for hawksbill turtles (Supplementary Material – Section F). Earlier studies had previously identified 47 green and 62 hawksbill nesting sites in the entire Red Sea (Supplementary Material – Section F). In total, we compiled data on clutches, emer- gences, and individual nesting turtles from 78 green and 110 hawksbill rookeries in the Red Sea where turtle nesting was confirmed between 1976 and 2020. From this data, we provide a revised overview of sea- sonality, distribution, and abundance of the sea turtles in the Red Sea. Details of new and published data are summarised in Supplementary Material – Section F.
3.1. Seasonality
3.1.1. Green turtles In NEOM – Amaala, nesting of green turtles was confirmed between
22 May and 9 October with the peak estimated in early August (Fig. 2a, Supplementary Material – Section D). In TRSP – Ras Al Baridi, green turtles nested between 21 April and 27 November with the peak esti- mated around mid-August (Fig. 2c, Supplementary Material – Section D). Green turtles appear to nest slightly earlier with a peak in July/ August at Zabargad Island, Egypt (Hanafy and Sallam, 2003; cited in Hanafy, 2012), which is another major rookery of green turtles in the Red Sea located approximately 150–230 km south-west of the Saudi Arabian sites (Fig. 3).
3.1.2. Hawksbill turtles In NEOM – Amaala, nesting of hawksbill turtles was observed be-
tween 22 May and 30 June with the peak likely around late May to early June (Fig. 2b, Supplementary Material – Section D), implying their nesting season starts in early May or possibly in April. In the TRSP – Ras Al Baridi region, we found evidence of hawksbill turtles nesting between 13 April and 29 July. Additionally, both adult male and female hawksbills were seen frequently in early March in the shallow waters adjacent to the nesting beaches within TRSP, although no surveys were possible between late March and mid-April due to logistical difficulties. This combined evidence suggests that in TRSP – Ras Al Baridi, hawksbill turtles likely start nesting in early April through July with the peak in late May and early June (Fig. 2d, Supplementary Material – Section D).
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Fig. 2. Cumulative distribution functions of Normal distribution (line) with the 95% confidence intervals (yellow bands), and cumulative nest abundance as pro- portion to the total clutch counts (points) for green and hawksbill turtles at (a, b) NEOM – Amaala, and (c, d) TRSP – Ras Al Baridi. Ticks along the x axes show the first date of each month. Note clutch counts and the associated dates were estimated from count data of clutches and emergences as described in Supplementary Material – Section C and main text. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 3. Nesting seasons of green and hawksbill turtles in the Red Sea. Lighter colours indicate nesting activities in each month (shown by a capital letter above each box) with darker colours denoting the peak periods. Months in bold mean that the presence or absence of nesting activities was confirmed by our field survey during the current study and from satellite tracking data from Shimada et al. (2021). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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Published studies on nesting seasonality of hawksbill turtles in the Red Sea at Giftun Islands in Egypt (Hanafy and Sallam, 2003; cited in Hanafy, 2012), Mukawwar Island and Suakin Archipelago in Sudan (PERSGA/GEF, 2007), Juzur2 Farasan in Saudi Arabia (PERSGA/GEF, 2007), and the Dahlak Archipelago in Eritrea (Eritrean Department of Environment, 2014), together with our new data, suggested latitudinal effects on seasonality of the nesting events (Fig. 3). Hawksbill turtles began nesting in December with a peak from February to April on the southern rookeries at Dahlak Archipelago, whereas nesting did not begin until May with a peak in June on the northern rookeries at Amaala, Giftun Islands, and NEOM, showing a clear delay in nesting activity with increasing latitude (Fig. 3).
3.2. Distribution and abundance
3.2.1. Green turtles Major rookeries of green turtles are aggregated in the northern Red
Sea between 24.60N and 25.63N (Fig. 4). The largest aggregation was found at Ras Al Baridi with annual estimates of 178 (95% CI = 121–362) and 330 (95% CI = 225–675) nesting individuals in 2018 and 2019 respectively (Fig. 4, Supplementary Material – Section F). The second largest aggregation occurred within TRSP, where a total of 185 turtles (95% CI = 101–604) were estimated to have nested in 2018 across 16 islands (Fig. 4, Supplementary Material – Section F). Approximately 61% of the nesting within TRSP occurred at Jazirat Mashabah with the abundance estimated at 113 (95% CI = 80–219) and 179 (95% CI = 122–367) nesting turtles in 2018 and 2019 respectively. At NEOM, across six island and one mainland sites combined, a total of 58 green turtles (95% CI = 18–321) were estimated nesting in 2018 (Fig. 4, Supplementary Material – Section F). This is probably a conservative estimate since two potential rookeries at Jazirat Thiran and Jazirat Sanafir could not be surveyed. From El-Sadek et al. (2016) we estimated that 62–168 (mean = 110) green turtles nested annually between 2009 and 2014 in Zabargad Island (Fig. 4, Supplementary Material – Section F). On other rookeries in the Red Sea, the mean number of nesting green turtles appears to be less than 50 individuals per annum (Fig. 4, Sup- plementary Material – Section F).
3.2.2. Hawksbill turtles Aggregations of >50 nesting hawksbill turtles occur in both the north
and south of the Red Sea. In the northern Red Sea, the largest aggre- gation was found at TRSP where we estimated 183 hawksbill turtles (95% CI = 152–217) nested in 2018 across 37 islands, with 79 of these (95% CI = 77–84) or 43% nesting at Jazirat Al Waqqadi. At NEOM, a total of 65 hawksbills (95% CI = 62–69) were estimated nesting in 2018 across 10 sites (8 island and 2 mainland), with approximately 67% of nesting occurring at Jazirat Shushah and Jazirat Walah (Fig. 4, Sup- plementary Material – Section F). Similar to green turtles, the actual abundance of nesting hawksbill turtles in NEOM is likely greater because two potential nesting sites were inaccessible for survey (Jazirat Thiran and Jazirat Sanafir). Other large aggregations of nesting hawksbill tur- tles have been reported to occur in the southern part of the Red Sea. Moore and Balzarotti (1977; cited in Groombridge and Luxmoore, 1989) estimated that approximately 330 hawksbill turtles nested at Suakin Archipelago in 1976. In 1983 Ormond et al. (1984) surveyed the Saudi Arabian coast of the Red Sea and found nests of hawksbill turtles on 48 islands. The largest of these were at Jazirat Marrak and Jazirat Dohrab (part of Juzur Farasan), where we estimated from nest count data that 73 (range 37 to 110) hawksbill turtles nested at each island that year. In Eritrea, at least 47 and 96 hawksbills nested on the rookeries within Dahlak Archipelago in 2006 and 2007 respectively (Teclemariam et al., 2009). On other islands and mainland rookeries of the Red Sea, the number of hawksbill turtles nesting annually was estimated to be less
than 50 individuals (Fig. 4, Supplementary Material – Section F).
3.2.3. Other sea turtles There is only one reported incidence of nesting by an olive ridley
turtle (Lepidochelys olivacea) in the Red Sea, on the southern coast of Eritrea (Pilcher et al., 2006). All other confirmed cases of nesting in the Red Sea were of green and hawksbill turtles (Supplementary Material – Section F).
3.3. Abundance trends
From the current study and the literature, we synthesised data collected at 10 green turtle rookeries and 12 hawksbill turtle rookeries in the Red Sea, where annual abundance data are available for more than one year.
3.3.1. Green turtles Ras Al Baridi is one of the most surveyed nesting sites of green turtles
in the Red Sea. The abundance of nesting females was first estimated in 1983 (Ormond et al., 1984), followed by more comprehensive studies between 1987 and 1995 (Al-Merghani et al., 2000). The current study provides the most recent estimates from the 2018 and 2019 nesting seasons. This combination of historical and new data provides abun- dance estimates from Ras Al Baridi across 11 nesting seasons between 1983 and 2019. Additionally, six other sites that Ormond et al. (1984) visited in 1983 were also monitored during the current study (Supple- mentary Material – Section F). Nesting was also reported for 12 seasons at Zabargad Island between 2001 and 2014 (El-Sadek et al., 2016; Hanafy, 2012).
The annual abundance of nesting green turtles appears to have increased since 1980–90s at Ras Al Baridi. We estimated that, on average, 43 green turtles nested between 1982 and 1995, whereas 254 individuals nested annually between 2018 and 2019 (Fig. 5, Supple- mentary Material – Section F). An increase was also apparent at Jazirat Mashabah, where the mean annual abundance estimate of 10 in- dividuals in 1983 increased to 146 turtles between 2018 and 2019 (Fig. 5, Supplementary Material – Section F). At other rookeries, the trend in nesting suggests stable or slightly increasing numbers (Fig. 5, Supplementary Material – Section F).
3.3.2. Hawksbill turtles Nine hawksbill turtle rookeries in Saudi Arabia were surveyed in
1983 (Ormond et al., 1984) and then again in 2018–2019 (this study). Along the western side of the Red Sea, several years of abundance data were reported from Giftun Islands, Egypt (Hanafy, 2012), and two years of data from Mojeidi Island, Eritrea (Teclemariam et al., 2009).
There was an apparent increase in the annual abundance of nesting hawksbill turtles at Jazirat Al Waqqadi, Saudi Arabia from 14 in- dividuals in 1983 to 79 individuals in 2018 (Fig. 5, Supplementary Material – Section F). Surveys at Big Giftun Island also showed a small increase in numbers during the 2000s with 6 individuals nesting in 2001 and 31 nesting in 2007 (Fig. 5, Supplementary Material – Section F). At Ras Al Baridi, where no hawksbill turtles had been recorded from 1983 to 1995 (Al-Merghani et al., 2000; Ormond et al., 1984), four fresh tracks of hawksbill turtles were recorded in June 2019. A decline in nesting was suggested at Jazirat Bargan, Saudi Arabia, with the esti- mates of 41 individuals in 1983 but only 3 individuals in 2018 (Fig. 5, Supplementary Material – Section F). Overall, at some locations nesting by hawksbill turtles appear to be stable or have increased since the 1980s, whereas other nesting aggregations may be in decline (Fig. 5, Supplementary Material – Section F).
4. Discussion
Using long term data sets and a novel approach to analysis, we have provided a comprehensive overview of the seasonality, distribution, and 2 ‘Juzur’ is the Arabic word for ‘islands of’.
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abundance of nesting sea turtles in the Red Sea. Importantly, we have identified 40 new sites used for nesting (38 island and 2 mainland) and found evidence that, for at least at some rookeries, abundance of nesting females is likely to have increased over the last three decades. Addi- tionally, the timing of nesting has shifted in some rookeries, possibly as a response to climate change.
Annual patterns in the abundance of nesting sea turtles must be interpreted with care. As shown at Ras Al Baridi and elsewhere in the world, numbers in proximate years almost always fluctuate regardless of the overall trend in the population (Al-Merghani et al., 2000; Chaloupka et al., 2008). The breeding biology of females and their foraging envi- ronment are two important elements that dictate these changes in numbers. Sea turtles are capital breeders and an adult female typically requires more than one year to attain a body condition suitable to pro- duce eggs (Miller, 1997). The time required to accumulate these energy reserves depends on the accessibility and quality of food, which in turn is largely influenced by environmental conditions. As a result, there is often synchronicity between the timing of breeding and climatic events that drive patterns of productivity. For example, in the Pacific Ocean, breeding of green turtles is correlated with El Nino-Southern Oscillation events (Limpus and Nicholls, 2000; Santidrian Tomillo et al., 2020). For any breeding population, the cycle of annual fluctuations in abundance of nesting females roughly equates to the average interval between two consecutive breeding seasons, which in general is 3–6 years for green and hawksbill turtles (Miller, 1997). However, the changes in numbers of nesting females that we observed across decades at some of the major rookeries in the Red Sea (Ras Al Baridi, Jazirat Mashabah, Jazirat Al Waqqadi) were still much larger than might be expected for typical annual fluctuations. For example, annual abundance of green turtles at Ras Al Baridi was much greater in 2018 and 2019 (178 and 330 in- dividuals, respectively) than any fluctuations observed between 1983 and 1995 (range 17 to 105 individuals), implying an increase in abun- dance over the two decades. Similarly, at Jazirat Al Waqqadi, the dif- ference in estimated abundances of hawksbill turtles between 1983 (14
individuals) and 2018 (79 individuals) were beyond the expected annual fluctuations for this species, which typically do not vary more than two- fold across proximate years (Bell et al., 2020). Additionally, our esti- mates of annual abundance are likely to be conservative measures, since some nests and tracks at these major rookeries may have become obscured prior to the surveys. Although our results must be interpreted with caution, particularly since many of the surveys in 1980/90s were short-term (sometimes involving only brief visits to beaches that may not have detected intermittent nesting), overall the weight of evidence suggests that populations at Ras Al Baridi, and potentially at two islands (Mashabah, Al Waqqadi), have indeed increased in abundance over the last three decades. This may be the result of management measures put in place in other areas of the population range across the Red Sea, since no formal protection had been given to nesting sites in Saudi Arabia (Mancini et al., 2015).
The occurrence of females at sites where nesting activities have not been reported previously (e.g. hawksbills at Ras Al Baridi) might be interpreted as further evidence for increases in population size. How- ever, it is important to note that except for Ras Al Baridi, many sites were surveyed very infrequently in the past, so that evidence of nesting ac- tivities might not have been detected. It is also possible that some turtles might have temporarily shifted their nesting sites, although such movements are infrequent (Limpus and Miller, 2008; Shimada et al., 2021). While bearing these caveats in mind, the new nesting sites identified in this study are located within the area of long-established rookeries of the species, suggesting that if indicative of increasing populations, recolonisation into parts of former ranges is occurring rather than expansion of nesting into new habitats. Hawksbill and green turtles have been severely exploited for shells, eggs and meat across the globe including the Red Sea (Mancini et al., 2015), but since the implementation of conservation strategies in many places, some pop- ulations have shown signs of recovery in abundance (Chaloupka et al., 2008; Hanafy, 2012) and may be recolonising former ranges. Such recolonisation is a phenomenon common to population recovery of both
Fig. 4. Distribution and estimated abundance of nesting (a) green and (b) hawksbill turtles in the Red Sea. The size and colour of each bubble are relative to the estimated annual number of nesting females at each site. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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aquatic and terrestrial fauna (Chapron et al., 2014; Lafferty and Tinker, 2014).
Our results show that the nesting seasons of sea turtles begins some months earlier in the south than in the north of the Red Sea, likely due to latitudinal-driven changes in temperatures. The Red Sea extends from 12.5 to 30N and the difference in water temperatures across this range of latitudes could be >5C (Agulles et al., 2020). Low temperatures can slow down or cease the development of turtle embryos, whereas expo- sure to very high temperatures (>~35C) will be lethal (Howard et al., 2014). In the warmer southern Red Sea, the optimal incubation tem- perature (~29C; Howard et al., 2014) likely occurs in late winter and spring, whereas in the cooler northern Red Sea, optima may not be achieved until the summer arrives some months later. Such differences may have implications for the timing (and potentially spatial distribu- tion) of breeding under global warming.
The effects of rising temperatures may also explain the apparent shifts in seasonality of nesting by sea turtles over decades. In 2019, nesting by green turtles at Ras Al Baridi started as early as April with the peak in August, whereas in the 1980s to early 1990s nesting only began in July/August with a peak in September/October (Al-Merghani et al., 2000; Pilcher and Al-Merghani, 2000; this study). This change has been accompanied by warming of the Red Sea over the last half century, which has trended upwards in temperature at a rate of 0.045 ± 0.016C per decade at 15 m depths (Agulles et al., 2020). Just off the coast of Ras Al Baridi (24.125N, 37.625E), the mean sea surface temperature was 26.1C in 1983 but averaged 27.7C in 2019 (National Centers for
Environmental Information, 2016). These warming trends may have driven turtles to now commence nesting earlier in a breeding season than a few decades in the past, a pattern consistent with changes in the timing of breeding seasons in response to changes in temperatures across a wide range of species (Mazaris et al., 2009; Visser et al., 2009). Relocation of nesting grounds to cooler environments could be an alternative response to warming temperatures but is rare in species that have fixed breeding sites, presumably because it is riskier to breed in a new, unknown habitat than to shift the timing of breeding at the same site. This emphasises the importance of the conservation of long-term nesting beaches for sea turtles in the Red Sea.
Spatially explicit management strategies can be highly effective for the conservation of sea turtles given their strong fidelity to nesting beaches and inter-nesting habitats (Jensen et al., 2013; Shimada et al., 2021). We identified nesting beaches that are critical for the sustain- ability of these endangered species in the Red Sea. Although the trend of increasing abundances at some nesting aggregations are encouraging, other rookeries had declining numbers of females and most populations are likely facing new and persistent anthropogenic threats including climate change, coastal development and beach armouring, pollution, both targeted and incidental catch in fisheries, and tourism (Hamann et al., 2010; Phillott and Rees, 2019). For this reason, it is important that the key nesting beaches receive comprehensive protection and that in- formation from older surveys of important aggregation sites of nesting females (e.g. Suakin Archipelago, Juzur Farasan) is updated to assess the potential impacts of these escalating threats.
Fig. 5. Annual abundance of nesting (a) green and (b) hawksbill turtles since 1983 in the Red Sea. Dashed lines connect data points of each site. See the Materials and Methods and Supplementary Material – Section F for details of how the abundance of nesting females were estimated. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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The results from our 2018–2019 surveys have already had a positive influence on conservation management of sea turtles. For example, Jazirat Al Waqqadi, one of the major rookeries of the hawksbill turtles in the Red Sea, has been entirely exempted from development and receives greater protection by the managing body (The Red Sea Development Company). Developments occurring nearby on other significant rook- eries such as Jazirat Mashabah, are also being carefully planned to avoid loss of important habitats and to mitigate impacts such as light pollution on nesting turtles and hatchlings. Other major rookeries, notably Ras Al Baridi, still have no formal systems of management in place to protect breeding populations of turtles. Given existing and predicted anthro- pogenic pressures (Pilcher, 1999; Shimada et al., 2021), it is highly desirable that Ras Al Baridi and other important sea turtle nesting habitats in the Red Sea are monitored regularly and receive compre- hensive protection.
CRediT authorship contribution statement
Mark G. Meekan: Resources; Writing - Review & Editing; Supervi- sion; Project administration; Funding acquisition.
Robert Baldwin: Conceptualisation; Methodology; Investigation; Writing - Original draft preparation; Writing - Review & Editing; Su- pervision; Project administration.
Abdulaziz M. Al-Suwailem: Resources; Supervision; Project administration; Funding acquisition.
Christopher Clarke: Investigation; Writing - Review & Editing; Supervision; Project administration.
August S. Santillan: Investigation. Carlos M. Duarte: Conceptualisation; Resources; Writing - Review &
Editing; Supervision; Project administration; Funding acquisition.
Ethics
No ethics approval was required to conduct the research as data collection did not involve interactions with the animals.
Funding
This research was funded by The Red Sea Development Company (TRSDC), Amaala, Beacon Development Company (BDC), King Abdullah University of Science and Technology (KAUST), and Australian Institute of Marine Science.
Declaration of competing interest
No conflict to declare.
Acknowledgments
We thank staff and numerous volunteers of TRSDC, Amaala, NEOM, BDC and KAUST for their support, in particular Reny Devassy, Abhish- ekh Vijayan, Raied A. Ajahdali, James Massey, Tito P. Pancho, and Zaki Al Jahdali. We also thank Jeffrey D. Miller and Nicolas Pilcher for their valuable advice and sharing key literature, M. Hamann for sharing raw data from Limpus et al. 2001, and Sea Turtle Association of Japan for sharing unpublished data.
Appendix A. Supplementary material
Supplementary material of this article can be found online at https ://doi.org/10.1016/j.biocon.2021.109235.
References
Agulles, M., Jorda, G., Jones, B., Agustí, S., Duarte, C.M., 2020. Temporal evolution of temperatures in the Red Sea and the Gulf of Aden based on in situ observations (1958–2017). Ocean Sci. 16, 149–166. https://doi.org/10.5194/os-16-149-2020.
Al-Merghani, M., Miller, J.D., Pilcher, N.J., Al-Mansi, A., 2000. The green and hawksbill turtles in the Kingdom of Saudi Arabia: synopsis of nesting studies 1986–1997. Fauna of Arabia 18, 369–384.
Baker, C.S., Steel, D., Calambokidis, J., Falcone, E., Gonzalez-Peral, U., Barlow, J., Burdin, A.M., Clapham, P.J., Ford, J.K.B., Gabriele, C.M., Mattila, D., Rojas- Bracho, L., Straley, J.M., Taylor, B.L., Urban, J., Wade, P.R., Weller, D., Witteveen, B. H., Yamaguchi, M., 2013. Strong maternal fidelity and natal philopatry shape genetic structure in North Pacific humpback whales. Mar. Ecol. Prog. Ser. 494, 291–306. https://doi.org/10.3354/meps10508.
Bell, I.P., Meager, J.J., Eguchi, T., Dobbs, K.A., Miller, J.D., Madden Hof, C.A., 2020. Twenty-eight years of decline: nesting population demographics and trajectory of the north-east Queensland endangered hawksbill turtle (Eretmochelys imbricata). Biol. Conserv. 241, 108376 https://doi.org/10.1016/j.biocon.2019.108376.
Campbell, L.M., 2003. Contemporary culture, use, and conservation of sea turtles. In: Lutz, P.L., Musick, J.A., Wyneken, J. (Eds.), The Biology of Sea Turtles, vol. II. CRC Press, Boca Raton, FL, pp. 307–338.
Chaloupka, M., Bjorndal, K.A., Balazs, G.H., Bolten, A.B., Ehrhart, L.M., Limpus, C.J., Suganuma, H., Troeeng, S., Yamaguchi, M., 2008. Encouraging outlook for recovery of a once severely exploited marine megaherbivore. Glob. Ecol. Biogeogr. 17, 297–304. https://doi.org/10.1111/j.1466-8238.2007.00367.x.
Chapron, G., Kaczensky, P., Linnell, J.D.C., Arx, M. von, Huber, D., Andren, H., Lopez- Bao, J.V., Adamec, M., Alvares, F., Anders, O., Balciauskas, L., Balys, V., Bedo, P., Bego, F., Blanco, J.C., Breitenmoser, U., Brøseth, H., Bufka, L., Bunikyte, R., Ciucci, P., Dutsov, A., Engleder, T., Fuxjager, C., Groff, C., Holmala, K., Hoxha, B., Iliopoulos, Y., Ionescu, O., Jeremic, J., Jerina, K., Kluth, G., Knauer, F., Kojola, I., Kos, I., Krofel, M., Kubala, J., Kunovac, S., Kusak, J., Kutal, M., Liberg, O., Majic, A., Mannil, P., Manz, R., Marboutin, E., Marucco, F., Melovski, D., Mersini, K., Mertzanis, Y., Mysajek, R.W., Nowak, S., Odden, J., Ozolins, J., Palomero, G., Paunovic, M., Persson, J., Potocnik, H., Quenette, P.-Y., Rauer, G., Reinhardt, I., Rigg, R., Ryser, A., Salvatori, V., Skrbinsek, T., Stojanov, A., Swenson, J.E., Szemethy, L., Trajçe, A., Tsingarska-Sedefcheva, E., Vana, M., Veeroja, R., Wabakken, P., Wolfl, M., Wolfl, S., Zimmermann, F., Zlatanova, D., Boitani, L., 2014. Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346, 1517–1519. https://doi.org/10.1126/science.1257553.
Cristofari, R., Liu, X., Bonadonna, F., Cherel, Y., Pistorius, P., Maho, Y.L., Raybaud, V., Stenseth, N.C., Bohec, C.L., Trucchi, E., 2018. Climate-driven range shifts of the king penguin in a fragmented ecosystem. Nat. Clim. Chang. 8, 245–251. https://doi.org/ 10.1038/s41558-018-0084-2.
El-Sadek, I., Ahmed, M.I., Aamer, M.A., Mancini, A., Hanafy, M.H., 2016. Nesting activities of green turtles (Chelonia mydas) on the beaches of Zabargad Island, southern Egyptian Red Sea. Egypt. J. Aquatic Biol. Fish. 20, 29–37. https://doi.org/ 10.21608/ejabf.2016.11175.
Eritrean Department of Environment, 2014. The 5th National Report on the Implementation of the UNCBD. The State of Eritrea, Ministry of Land and Environment. Department of Environment, Asmara, Eritrea.
Esteban, N., Mortimer, J.A., Hays, G.C., 2017. How numbers of nesting sea turtles can be overestimated by nearly a factor of two. Proc. Roy. Soc. B: Biol. Sci. https://doi.org/ 10.1098/rspb.2016.2581.
Fuentes, M., Limpus, C.J., Hamann, M., Dawson, J., 2010. Potential impacts of projected sea-level rise on sea turtle rookeries. Aquat. Conserv. Mar. Freshwat. Ecosyst. 20, 132–139. https://doi.org/10.1002/aqc.1088.
Gronwald, M., Genet, Q., Touron, M., 2019. Predation on green sea turtle, Chelonia mydas, hatchlings by invasive rats. Pac. Conserv. Biol. 25, 423–424. https://doi.org/ 10.1071/PC18087.
Groombridge, B., Luxmoore, R., 1989. The green turtle and hawksbill (Reptilia: Cheloniidae): world status, exploitation and trade. CITES (Convention on International Trade in Endangered Species) Secretariat, Lausanne, Switzerland.
Groot, C., Margolis, L. (Eds.), 1991. Pacific Salmon Life Histories. UBC Press, Vancouver. Hamann, M., Godfrey, M.H., Seminoff, J.A., Arthur, K., Barata, P.C.R., Bjorndal, K.A.,
Bolten, A.B., Broderick, A.C., Campbell, L.M., Carreras, C., Casale, P., Chaloupka, M., Chan, S.K.F., Coyne, M.S., Crowder, L.B., Diez, C.E., Dutton, P.H., Epperly, S.P., FitzSimmons, N.N., Formia, A., Girondot, M., Hays, G.C., Cheng, I.J., Kaska, Y., Lewison, R., Mortimer, J.A., Nichols, W.J., Reina, R.D., Shanker, K., Spotila, J.R., Tomas, J., Wallace, B.P., Work, T.M., Zbinden, J., Godley, B.J., 2010. Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger. Species Res. 11, 245–269. https://doi.org/10.3354/ esr00279.
Hanafy, M., 2012. Nesting of marine turtles on the Egyptian beaches of the Red Sea. Egypt. J. Aquatic Biol. Fish. 16, 59–71. https://doi.org/10.21608/ejabf.2012.2125.
Hanafy, M.H., Sallam, A., 2003. Status of Marine Turtles Nesting on the Egyptian Beaches of the Red Sea. PERSGA.
Howard, R., Bell, I., Pike, D.A., 2014. Thermal tolerances of sea turtle embryos: current understanding and future directions. Endanger. Species Res. 26, 75–86. https://doi. org/10.3354/esr00636.
IUCN, 2020. The IUCN red list of threatened species. Version 2020-3. [WWW Document]. URL https://www.iucnredlist.org (Accessed 12.22.20).
Jensen, M.P., FitzSimmons, N.N., Dutton, P.H., 2013. Molecular genetics of sea turtles, in: Wyneken, J., Lohmann, K.J., Musick, J.A. (Eds.), The Biology of Sea Turtles, Volume vol. III. CRC Press, Boca Raton, FL, pp. 135–161.doi:https://doi.org/10.12 01/b13895.
T. Shimada et al.
10
Jensen, M., Miller, J., FitzSimmons, N., Al-Merghani, M., 2019. Identification of Chelonia mydas populations in the Kingdom of Saudi Arabia through regional genetic analyses. Mar. Turt. Newsl. 16–20.
Kameda, K., Wakatsuki, M., 2011. Reproductive biology of the hawksbill turtle, Eretmochelys imbricata, on Kuroshima Island of Yaeyama group, Ryukyu archipelago. Umigame News Letter 12–14.
Lafferty, K.D., Tinker, M.T., 2014. Sea otters are recolonizing southern California in fits and starts. Ecosphere 5, art50. https://doi.org/10.1890/ES13-00394.1.
Laloe, J.-O., Cozens, J., Renom, B., Taxonera, A., Hays, G.C., 2017. Climate change and temperature-linked hatchling mortality at a globally important sea turtle nesting site. Glob. Chang. Biol. 23, 4922–4931. https://doi.org/10.1111/gcb.13765.
Limpus, C.J., Miller, J.D., 2008. Australian Hawksbill Turtle Population Dynamics Project. Environmental Protection Agency, Queensland.
Limpus, C., Nicholls, N., 2000. ENSO regulation of indo-Pacific green turtle populations. In: Hammer, G.L., Nicholls, N., Mitchell, C. (Eds.), Applications of Seasonal Climate Forecasting in Agricultural and Natural Ecosystems - the Australian Experience, pp. 399–408.
Limpus, C.J., Carter, D., Hamann, M., 2001. The green turtle, Chelonia mydas, in Queensland, Australia: the bramble cay rookery in the 1979-1980 breeding season. Chelonian Conserv. Biol. 4, 34–46.
Mancini, A., Elsadek, I., El-Alwany, M.A.N., 2015. Marine turtles of the Red Sea. In: Rasul, N.M.A., Stewart, I.C.F. (Eds.), The Red Sea: The Formation, Morphology, Oceanography and Environment of a Young Ocean Basin, Springer Earth System Sciences. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp. 551–565. https://doi. org/10.1007/978-3-662-45201-1_31.
Mancini, A., Phillott, A., Rees, A.F., 2019. Chelonia mydas North Indian Ocean subpopulation. In: IUCN Red List of Threatened Species. https://doi.org/10.2305/ IUCN.UK.2019-2.RLTS.T142121108A154845002.en.
Mashat, A., Abdel Basset, H., 2011. Analysis of rainfall over Saudi Arabia. JKAU: Met., Env. & Arid Land Agric. Sci 22, 59–78.doi:https://doi.org/10.4197/Met. 22–2.4.
Mazaris, A.D., Kallimanis, A.S., Tzanopoulos, J., Sgardelis, S.P., Pantis, J.D., 2009. Sea surface temperature variations in core foraging grounds drive nesting trends and phenology of loggerhead turtles in the Mediterranean Sea. J. Exp. Mar. Biol. Ecol. 379, 23–27. https://doi.org/10.1016/j.jembe.2009.07.026.
Mazaris, A.D., Schofield, G., Gkazinou, C., Almpanidou, V., Hays, G.C., 2017. Global sea turtle conservation successes. Sci. Adv. 3, e1600730 https://doi.org/10.1126/ sciadv.1600730.
Miller, J.D., 1997. Reproduction in sea turtles, in: Lutz, P.L., Musick, J.A. (Eds.), The Biology of Sea Turtles, Volume vol. I. CRC Press, Boca Raton, FL, pp. 51–81.doi: https://doi.org/10.1201/9780203737088.
Moore, R.J., Balzarotti, M.A., 1977. Report of 1976 expedition to Suakin Archipelago (Sudanese Red Sea). Results of marine turtle survey and notes on marine and bird life.
Mortimer, J.A., Camille, J.-C., Boniface, N., 2011. Seasonality and status of nesting hawksbill (Eretmochelys imbricata) and green turtles (Chelonia mydas) at D’Arros Island, Amirantes group, Seychelles. Chelonian Conserv. Biol. 10, 26–33. https:// doi.org/10.2744/CCB-0830.1.
National Centers for Environmental Information, 2016. GHRSST level 4 AVHRR_OI global Blended Sea surface temperature analysis (GDS version 2) from NCEI. Ver. 2. PO.DAAC, CA, USA [WWW Document]. URLdoi:10.5067/GHAAO-4BC02 (accessed 7.24.20).
Okuyama, J., Ishii, H., Tanizaki, S., Suzuki, T., Abe, O., Nishizawa, H., Yano, A., Tsujimura, M., Ishigaki, Takakazu, Ishigaki, Takashi, Kobayashi, M., Yanagida, H., 2020. Quarter-century (1993–2018) nesting trends in the peripheral populations of three sea turtle species at Ishigakijima Island, Japan. ccab 19, 101–110. https://doi. org/10.2744/CCB-1428.1.
Ormond, R.F.G., Dawson-Sheppard, A., Price, A., Pitts, R.G., 1984. Report on the Distribution of Habitats and Species in the Saudi Arabian Red Sea. International Union for Conservation of Nature/Meteorological and Environmental Protection Administration/PERSGA, Kingdom of Saudi Arabia.
Pendoley, K., Kamrowski, R.L., 2016. Sea-finding in marine turtle hatchlings: what is an appropriate exclusion zone to limit disruptive impacts of industrial light at night? J. Nat. Conserv. 30, 1–11. https://doi.org/10.1016/j.jnc.2015.12.005.
PERSGA/GEF, 2007. Regional action plans for the conservation of marine turtles, seabirds and mangroves in the Red Sea and Gulf of Aden (No. 12). In: PERSGA Technical Series. PERSGA, Jeddah, Saudi Arabia.
Phillott, A.D., Rees, AL.F., 2019. Sea Turtles in the Middle East and South Asia Region MTSG Annual Regional Report 2019 (Report of the IUCN-SSC Marine Turtle Specialist Group).
PIF, 2017. The Public Investment Fund Program (2018–2020). Public Investment Fund. Pilcher, N.J., 1999. Cement dust pollution as a cause of sea turtle hatchling mortality at
Ras Baridi, Saudi Arabia. Mar. Pollut. Bull. 38, 966–969. https://doi.org/10.1016/ S0025-326X(99)00110-1.
Pilcher, N.J., Al-Merghani, M., 2000. Reproductive biology of green turtles at Ras Baridi, Saudi Arabia. Herpetol. Rev. 31, 142–147.
Pilcher, N., Mahmud, S., Howe, S., Teclemariam, Y., Weldeyohannes, S., 2006. An update on Eritrea’s marine turtle programme and first record of olive ridley turtle nesting in the Red Sea. Mar. Turt. Newsl. 16.
Pilcher, N.J., Antonopoulou, M., Perry, L., Abdel-Moati, M.A., Al Abdessalaam, T.Z., Albeldawi, M., Al Ansi, M., Al-Mohannadi, S.F., Al Zahlawi, N., Baldwin, R., Chikhi, A., Das, H.S., Hamza, S., Kerr, O.J., Al Kiyumi, A., Mobaraki, A., Al Suwaidi, H.S., Al Suweidi, A.S., Sawaf, M., Tourenq, C., Williams, J., Willson, A., 2014. Identification of Important Sea turtle areas (ITAs) for hawksbill turtles in the Arabian region. J. Exp. Mar. Biol. Ecol. 460, 89–99. https://doi.org/10.1016/j. jembe.2014.06.009.
R Core Team, 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Santidrian Tomillo, P., Fonseca, L.G., Ward, M., Tankersley, N., Robinson, N.J., Orrego, C.M., Paladino, F.V., Saba, V.S., 2020. The impacts of extreme El Nino events on sea turtle nesting populations. Clim. Chang. 159, 163–176. https://doi. org/10.1007/s10584-020-02658-w.
Shimada, T., Limpus, C., Jones, R., Hamann, M., 2017. Aligning habitat use with management zoning to reduce vessel strike of sea turtles. Ocean Coast. Manag. 142, 163–172. https://doi.org/10.1016/j.ocecoaman.2017.03.028.
Shimada, T., Limpus, C.J., Hamann, M., Bell, I., Esteban, N., Groom, R., Hays, G.C., 2020. Fidelity to foraging sites after long migrations. J. Anim. Ecol. 89, 1008–1016. https://doi.org/10.1111/1365-2656.13157.
Shimada, T., Duarte, C.M., Al-Suwailem, A.M., Tanabe, L., Meekan, M.G., 2021. Satellite tracking reveals nesting patterns, site fidelity, and potential impacts of warming on major rookeries of green turtles in the Red Sea. Front. Mar. Sci. https://doi.org/ 10.3389/fmars.2021.633814.
Teclemariam, Y., Giotom, M., Mengstu, T., Abraha, H., Mahmud, S., 2009. An update on marine turtles in Eritrea, Red Sea. Indian Ocean Turtle Newsletter 6–10.
Venter, O., Sanderson, E.W., Magrach, A., Allan, J.R., Beher, J., Jones, K.R., Possingham, H.P., Laurance, W.F., Wood, P., Fekete, B.M., Levy, M.A., Watson, J.E.M., 2016. Sixteen years of change in the global terrestrial human footprint and implications for biodiversity conservation. Nat. Commun. 7, 12558–12558.doi:https://doi.org/ 10.1038/ncomms12558.
Visser, M.E., Holleman, L.J.M., Caro, S.P., 2009. Temperature has a causal effect on avian timing of reproduction. Proc. R. Soc. B Biol. Sci. 276, 2323–2331. https://doi.org/ 10.1098/rspb.2009.0213.
Wallace, B.P., DiMatteo, A.D., Hurley, B.J., Finkbeiner, E.M., Bolten, A.B., Chaloupka, M. Y., Hutchinson, B.J., Abreu-Grobois, F.A., Amorocho, D., Bjorndal, K.A., Bourjea, J., Bowen, B.W., Duenas, R.B., Casale, P., Choudhury, B.C., Costa, A., Dutton, P.H., Fallabrino, A., Girard, A., Girondot, M., Godfrey, M.H., Hamann, M., Lopez- Mendilaharsu, M., Marcovaldi, M.A., Mortimer, J.A., Musick, J.A., Nel, R., Pilcher, N.J., Seminoff, J.A., Troeng, S., Witherington, B., Mast, R.B., 2010. Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PloS One 5, e15465–e15465.doi: https://doi.org/10.1371/journal.pone.0015465.
Wheelwright, N.T., Mauck, R.A., 1998. Philopatry, natal dispersal, and inbreeding avoidance in an island population of Savannah sparrows. Ecology 79, 755–767. https://doi.org/10.1890/0012-9658(1998)079[0755:PNDAIA]2.0.CO;2.
T. Shimada et al.
1 Introduction
2.2 Published information
3 Results
3.1 Seasonality