The Persian Gulf (hereafter referred to as the Gulf) supports regionally and globally important (Wallace et al. 2010; Phillott and Rees 2021) nesting populations of hawksbill turtles (Eretmochelys imbricata) on the mainland beaches and/or islands of Iran (Mobaraki 2004a, 2004b; Loghmani et al. 2011; Hesni et al. 2019), Qatar (Supreme Council for the Environment and Natural Reserves [SCENR] 2006 in Pilcher et al. 2015), Saudi Arabia (Pilcher 1999; Al-Merghani et al. 2000), and the UAE (Al-Ghais 2009), with lower density nesting also occurring in Kuwait (Rees et al. 2018; Rees 2021). A semi-enclosed marine basin, the Gulf is one of the most extreme environments utilized by sea turtles. Hawksbill turtles nesting in the Gulf experience a significantly greater increase in ambient temperatures during the nesting season than most or all other populations worldwide and, potentially in response, nest during a shorter annual season. Clutches are already experiencing elevated incubation temperatures at levels predicted to occur in response to global warming at other locations in the second half of the 21st century, and significant female-biased sex ratios are likely to be realized by 2100 (Chatting et al. 2021).

When comparing the nesting ecology of hawksbill turtles in the Gulf with global populations, Chatting et al. (2018) examined turtle size (carapace length) and reproductive output (clutch size). Numbers of yolkless eggs were excluded from the study (Chatting et al. 2018), but comparatively high numbers of yolkless eggs have been reported from hawksbill turtles nesting across the northern Indian Ocean, including (from west to east) Seil Ada Kabir Island in Sudan (Hirth and Abdel Latif 1980), the Gulf of Aden (Hirth and Carr 1970), islands in the Egyptian Red Sea (Frazier and Salas 1984), Jabal Aziz Island in Yemen (Hirth and Carr 1970), Masirah Island in Oman (Ross 1980), and Gulf islands of Saudi Arabia (Pilcher 1999) and Kuwait (Rees et al. 2020).

Yolkless eggs were first described by Hughes et al. (1967) and have since been referred to by some researchers as shelled albumen gobs or globs (SAGs; Sotherland et al. 2003; Bell et al. 2004) because they are not “true” eggs. Yolkless eggs typically comprise granules of yolk too small to bear an embryonic disc, surrounded by albumen and enclosed in a thin shell. They are often irregularly shaped and < 50% of the diameter of a normal yolked egg, with no potential to produce a hatchling. Yolkless eggs are thought to comprise tissue debris formed after ovulation or fragments of a ruptured yolk that entered the oviduct and became enclosed in albumen and shell. They are laid by all species but are more common and numerous in clutches laid by leatherback turtles (Dermochelys coriacea; Miller 1985; Miller et al. 2003) and are often among the last to be laid during oviposition (Pritchard 1971; Miller 1985).

It is unclear whether yolkless eggs provide some adaptive advantage or are simply the accidental result of usual physiological processes with no specific role (Dutton and McDonald 1995), but the following possible functions have been postulated: a) sacrificial eggs to satiate or deter predators (Hirth 1980; Frazier and Salas 1984; Caut et al. 2006); b) provide thermal buffering (Frazier and Salas 1984, but see Wallace et al. 2004); c) act as moisture reservoirs (Hall 1990; Dutton and McDonald 1995; Wallace et al. 2006); d) create or ensure air spaces in the egg mass to facilitate gas exchange (Frazier and Salas 1984; Dutton and McDonald 1995; Williams 1996 in Wallace et al. 2004, but see Wallace et al. 2004); e) create space, through dehydration, to facilitate synchronous emergence of hatchlings (Patiño-Martinez et al. 2010); or, f) improve the hatching success of viable eggs through unknown means (Whitmore and Dutton 1985; Caut et al. 2006).

Frazier and Salas (1984) suggested that the large numbers of yolkless eggs laid by hawksbills in the Red Sea, Gulf of Aden, and Arabian Sea were the result of physiological (thermal) stress. The species is believed to have colonized the Gulf more recently than other locations throughout the Indo-Pacific, and populations in the area demonstrate genetic differentiations (Zolhgarnein et al. 2011; Tabib et al. 2014), despite some being separated by < 200 km (Vargas et al. 2016). So far, however, little is known about variability in body form and life history among these disparate populations. In this study, we compared the morphometrics of nesting hawksbill turtles and number of yolked and yolkless eggs from Iranian islands in the northern Gulf with other populations worldwide so as to understand the relationship between carapace length, reproductive output, and production of yolkless eggs.

METHODS

Morphometrics and Reproductive Output. — The field study occurred at Sheedvar, Hendourabi, Nakhiloo, and Ommolkaram islands (Table 1; Fig. 1). Each location was visited for 10–15 d in April–May, from 2005 to 2010 for Nakhiloo and Ommolkaram islands and 2005–2019 for Sheedvar and Hendourabi islands. All nesting beaches were monitored at night for nesting turtles; ∼ 20% of hawksbill turtles were recorded to nest from 0700 to 2000 hrs at these study sites, but daytime temperatures are challenging for field work and the majority of turtles are encountered at night. Once turtles had completed oviposition, the curved carapace length (notch to tip; CCL_nt), curved carapace width (CCW), and plastron length (PL) were measured to the nearest 1.0 cm, and total tail length (TTL) and postcloacal tail length (PTL) were measured to the nearest 0.5 cm using a flexible fiberglass tape (see Bolten 1999 for description of methodology). A hanging balance, suspended by a pole or by hand, was used to weigh turtles to the nearest 1.0 kg. Turtles were tagged with a uniquely numbered titanium Stockbrands© tag in the proximal left fore-flipper (see Balazs 1999).

Table 1. Characteristics of study locations for hawksbill turtles nesting on Iranian islands (Is.) in the northern Persian Gulf (from Mobaraki 2021).

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During each visit to a site, the total clutch count (number of yolked and multiyolked eggs; see Miller 1999) was recorded for all nesting turtles intercepted, and the number of yolkless eggs for 5–10 clutches. Finally, 15 eggs from each clutch were selected using nonsystematic sampling to be measured to the nearest 0.1 cm and weighed to the nearest 1.0 g using digital calipers and balance, respectively. All eggs were returned to the nest within 30 min of removal, with yolkless eggs returned to the nest after yolked eggs.

Morphometric and reproductive output data for these islands has not been previously reported and was closely examined for variation as genetic differences among nesting populations in the region have been described (Zolhgarnein et al. 2011; Tabib et al. 2014; Vargas et al. 2016). Data sets for each variable were checked for normality using a Kolmogorov-Smirnov test and Shapiro-Wilk test as appropriate, then variation among locations was examined using an analysis of variance (ANOVA) and post hoc Tukey test (for data with a normal distribution) with Cohen's f² to assess effect size, or Kruskal-Wallis test and Mann-Whitney U-test (for data without a normal distribution) with r or Cohen's d to indicate effect size as appropriate. Data from all locations were pooled to assess the significance of associations among variables of interest, including CCL, egg diameter and weight, and number of yolked and yolkless eggs, using linear regression. Statistical tests were performed using SPSS v27.

Meta-analysis of Global Hawksbill Turtle Morphometrics and Reproductive Output. — We used a similar approach to Chatting et al. (2018) in comparing CCL and clutch size from the current study with raw data from previously published studies and reports of global nesting populations. Digitized data were manually extracted from images using WebPlotDigitzer© (https://apps.automeris.io/wpd/). We converted different measurements of carapace length to CCL_nt using allometric equations for hawksbill turtles from van Dam and Diez (1998; Table S1; supplemental material can be found online at https://doi.org/10.2744/CCB-1546.1.s1).

There are 3 major differences in our treatment of data in comparison with Chatting et al. (2018). a) We converted the straight carapace length reported by Ross (1980) to CCL_nt differently (Table S1). b) We included only the number of yolked eggs (described in the original study as “fertile eggs”) in clutch size from Hirth (1980). In contrast, Chatting et al. (2018) included both yolked and yolkless eggs. (Note also that data from Hirth [1980] were erroneously attributed to Hirth and Abdel Latif [1980] in Chatting et al. [2018].) c) We included all relevant data from Pilcher et al. (2014a) whereas Chatting et al. (2018) did not include CCL of turtles at Fuwairit, Qatar.

A one-way ANOVA was used to compare each variable among regions (Gulf, Gulf of Oman, Arabian Sea, Red Sea, Caribbean, West Atlantic, and Southwest Pacific). Post hoc Tukey tests were utilized to identify differences where appropriate, and Eta squared (η²) was calculated to measure effect size. Statistical tests were performed using SPSS v27.

Comparison of Global Hawksbill Turtle Yolkless Egg Counts. — Raw data on the number of yolkless eggs laid by individual turtles is only reported in studies from the region (Hirth 1980; Ross 1980) so this variable could not be included in the meta-analysis. However, mean counts reported from different populations worldwide were summarized for comparison.

RESULTS

Morphometrics and Reproductive Output. — Morphometrics of nesting hawksbill turtles, clutch counts, and characteristics of eggs at the 4 study locations are presented in Table 2. Total tail length of nesting turtles, diameter and weight of yolked eggs, and the number of yolkless eggs per clutch demonstrated significant variation among locations. Pairwise comparisons detected significant differences in variables among locations, but the effect size was moderate or less (r < 0.5 or d < 0.8; Table 3). Hence, data from the 4 islands were pooled for the meta-analysis of global hawksbill turtle morphometrics and reproductive output.

Table 2. Variation in morphometrics of hawksbill turtles and their eggs from Iranian islands (Is.) in the Persian Gulf. Analysis of variance (ANOVA) applied to data sets with a normal distribution and Kruskal-Wallis test to data without a normal distribution. Significant variation at α = 0.05 is indicated by an asterisk (*).

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Table 3. Pairwise comparisons among study locations (Is. = Island) for variables total tail length, and diameter and weight of yolked eggs, of hawksbill turtles in the Persian Gulf. Tukey test applied to data sets with a normal distribution and Mann-Whitney U-test to data without a normal distribution. Significant variation at α = 0.05, and large effect size are indicated by an asterisk (*): r (Mann-Whitney U effect size): < 0.1 negligible, 0.1–0.3 small effect, 0.3–0.5 moderate effect, > 0.5 large effect; Cohen's d (effect size): < 0.2 negligible, 0.2–0.5 small effect, 0.5–0.8 moderate effect, > 0.8 large effect (Cohen 1988, 1992).

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The diameter, weight, and number of yolked eggs per clutch increased significantly with CCL (Table 4); however, the effect size was only large for number of yolked eggs (f² = 0.152). No significant relationship between CCL and the number of yolkless eggs, or the number of yolked and yolkless eggs (Table 4), was shown by regression analysis.

Table 4. Variation in reproductive output of nesting hawksbill turtles from Iranian islands in the Persian Gulf. Significant variation at α = 0.05 and large effect size are indicated by an asterisk: Cohen's f² (effect size): < 0.02 small effect, 0.02–0.15 medium effect, 0.15–0.35 large effect (Cohen 1988, 1992). CCL = curved carapace length.

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Meta-analysis of Global Hawksbill Turtle Morphometrics and Reproductive Output. — Significant variation in CCL (F_6,955 = 1166.730, p = 0.000) and number of yolked eggs (F_3,580 = 310.706, p < 0.001; η² = 0.616) occurred among regions, with a very large effect size (η² = 0.880 and 0.616) in both analyses. Post hoc analyses indicated that hawksbill turtles from the Gulf were smaller than those in the Gulf of Oman (p < 0.001), Arabian Sea (p = 0.000), Caribbean (p = 0.000), West Atlantic (p = 0.000), and Southwest Pacific (p = 0.000) but not the Red Sea (p = 0.104; see also Fig. 2). Similarly, hawksbill turtles in the Gulf laid fewer yolked eggs than populations in the Caribbean (p < 0.001), and West Atlantic (p = 0.001) but not the Red Sea (p = 0.636; see also Fig. 3).

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Comparison of Global Hawksbill Turtle Yolkless Egg Counts. — A comparison of summary data (Fig. 4) suggests that clutches laid by hawksbill turtle populations nesting in the Gulf and Red Sea, and potentially the Arabian Sea include a larger number of yolkless eggs than populations nesting elsewhere in the world. Yolkless eggs are usually so few in hawksbill turtle nests that some studies report only the number or percentage of nests examined that contained yolkless eggs instead of the number of yolkless eggs per clutch. For example, Witzell and Banner (1980) found only 1–3 yolkless eggs in 3 clutches of 23 examined in Samoa, and Wood (1986) found no more than 2 yolkless eggs in each of 4 nests from 127 in total in the Seychelles.

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DISCUSSION

Morphometrics and Reproductive Output. — Significant differences in some morphometrics (total tail length) and egg characteristics (diameter and weight of yolked eggs, and the number of yolkless eggs per clutch) were detected among populations nesting on Iranian islands in the northern Gulf but these had moderate or less effect sizes (Table 4) and we do not consider them to be biologically relevant. Nakhiloo and Ommolkaram islands, and Hendourabi and Sheedvar islands, are within < 50 km of each other and strong site fidelity of nesting populations at these islands, as demonstrated by hawksbills turtles nesting in Australia (Hoenner et al. 2016), Brazil (Santos et al. 2016), Caribbean (Richardson et al. 1999), Costa Rica (Bjorndal et al. 1985), Cuba (Moncada et al. 2010, 2012), Puerto Rico (Diez and Van Dam 2007; but not in the Caribbean [Kendall et al. 2019] or Mexico [Garduño-Andrade 1999]), may have contributed to known genetic differences (Zolhgarnein et al. 2011; Tabib et al. 2014; Vargas et al. 2016) and local morphometric variations detected in this study.

Meta-analysis of Global Hawksbill Turtle Morphometrics and Reproductive Output. — Similar to Chatting et al. (2018), we also found hawksbill turtles from the Gulf and Red Sea to be smaller in carapace length than other hawksbill populations at a global scale (Fig. 2). Chatting et al. (2018) concluded that this did not indicate a nesting population comprising younger (i.e., smaller) adults because size was consistent over their 7-yr study period and the maximum CCL recorded was 74.0 cm. Instead, Chatting et al. (2018) attributed the comparatively smaller size to low habitat productivity and foraging success. Unfortunately, published data sets are not available to detect temporal declines in somatic growth rates, as observed in West Atlantic hawksbill turtles as a result of declining foraging resources (Bjorndal et al. 2016). We note that comparatively small body size of hawksbill turtles in the Gulf and Red Sea may also be due to occupation of high-temperature waters (Sheridan and Bickford 2011).

Satellite telemetry studies indicate that nesting hawksbill turtles in the Gulf remain within their waters for foraging (Pilcher et al. 2014b; Rees et al. 2019; Marshall et al. 2020). Hawksbill turtles nesting in the Arabian Sea (Oman) have been tracked into the Gulf of Oman but rarely pass through the Strait of Hormuz to the Gulf (Pilcher et al. 2014a). This is in contrast to green (Chelonia mydas), loggerhead (Caretta caretta), and olive ridley (Lepidochelys olivacea) turtles tracked in the region, the majority of which do move between foraging and nesting habitat in the Gulf, Arabian Sea, and elsewhere in the northern Indian Ocean (Rees et al. 2010, 2012a, 2012b; Mobaraki et al. 2020; Pilcher et al. 2020, 2021). Hawksbill turtles nesting in the Gulf may be restricted to its waters through a) adaptation; b) physical limitations and the inability to navigate the currents that the other, larger species of sea turtles can transit to move between the Gulf and northern Indian Ocean (as occurs in immature loggerhead turtles in the Mediterranean Sea; Carreras et al. 2006); or c) a bottleneck/founder event (see Natoli et al. 2017; Arantes et al. 2020) that other sea turtles nesting in the Gulf and foraging outside the Gulf did not experience (Jensen et al. 2019) resulting in different postnesting migratory behavior/s.

The narrow Strait of Hormuz renders the Gulf a semi-enclosed sea, with extreme thermal variability and high salinity (Vaughan et al. 2019). These environmental conditions, and major coastal development in countries bordering the Gulf (as described in Al-Ghais 2009; Pilcher et al. 2014b, 2015), have implications for hawksbill foraging habitat. Many adult hawksbill turtles foraging in coastal waters of the Gulf undertake summer “migration loops” to deeper, cooler waters in the Gulf with low productivity and only return to shallower waters comprising patchy coral habitat after several months (September–October) when temperatures are 1.5°C–2.0°C cooler (Pilcher et al. 2014a; Marshall et al. 2020; but also see Rees et al. 2019).

No telemetry studies of nesting hawksbill turtles in the Red Sea have been published to determine whether their space use is as limited as those nesting in the Gulf. Limited tracking studies of other species nesting in the area have shown postnesting green turtles (Rees et al. 2012a; Pilcher et al. 2021) and olive ridleys (Rees et al. 2012b) migrating from Oman in the Arabian Sea into the Red Sea and postnesting loggerhead turtles to the Bab el-Mandeb Strait (Rees et al. 2010). As observed in the Gulf, some green turtles nesting on coastline of the Red Sea also remain in local waters when foraging (Attum et al. 2014; Al-Mansi et al. 2021). The Red Sea, too, is a semi-enclosed sea, with barriers including the narrow Strait of Bab el-Mandeb Strait that separates the Red Sea from the Gulf of Aden and cold-water upwelling between the Gulf of Aden and rest of the Arabian Sea (reviewed by DiBattista et al. 2016). Subadult and adult hawksbill turtles have been observed foraging throughout the Red Sea (PERSGA 2004; al Zibdah 2007; Mancini et al. 2015). Coral reef ecosystems in the Red Sea once considered productive (Riegl et al. 2012; DiBattista et al. 2016) are now in decline as a result of anthropogenic disturbance (see Riegl et al. 2012). Waters of the Red Sea experience extreme high salinity and temperatures, varying along a latitudinal gradient (Carvalho et al. 2019).

The small size of adult hawksbills in the Gulf and Red Sea may be caused by poor foraging habitat and/or extreme environmental conditions. Relationships between size and genetic characteristics are impossible to assess given that global studies of hawksbill turtles include samples from populations in the Gulf (Vargas et al. 2016; Reid et al. 2019) but not the Red Sea or Arabian Sea. The Gulf hawksbill turtle population is considered to have originated from a single founder event and subsequent population expansion (Natoli et al. 2017) so a genetic relationship seems unlikely, but a comparative study of wider populations in the northern Indian Ocean could aid understanding of factors resulting in smaller turtle size and consequent clutch count.

Whatever the driver, sea turtle size has implications for seasonal reproductive output (the number of yolked eggs). Positive relationships between female size and number of yolked eggs have been found in hawksbill (Pérez-Castañeda et al. 2007; this study), green (Bjorndal and Carr 1989; Hays et al. 1993; Johnson and Ehrhart 1996; Broderick et al. 2003), leatherback (Wallace et al. 2007; Le Gouvello et al. 2020), loggerhead (Frazer and Richardson 1986; Hays and Speakman 1991; Broderick et al. 2003; LeBlanc et al. 2014; Le Gouvello et al. 2020), and olive ridley (Gatto et al. 2020) turtles. Like Chatting et al. (2018), we found the number of yolked eggs laid by hawksbill turtles in the Gulf to be fewer than those of other populations worldwide, including those in the Gulf of Oman and Arabian Sea. However, unlike Chatting et al. (2018), our inclusion of only yolked eggs from Hirth (1980) in the meta-analysis resulted in finding no difference between hawksbill turtle clutch size in the Gulf and Red Sea (Fig. 3). Our findings of smaller body size and smaller clutch size in hawksbill turtle populations nesting in the Gulf and Red Sea supports the optimal egg size theory, in which larger turtles produce larger clutches but not larger eggs (Smith and Fretwell 1974). A meta-analysis of egg dimensions and weights from global hawksbill turtle populations (raw data unavailable; summary data in Table S2) could provide further insight.

Comparison of Global Hawksbill Turtle Yolkless Egg Counts. — The biological significance of yolkless eggs in hawksbill turtle clutches has not been previously studied and requires further attention, especially because clutches laid by turtles nesting in the Gulf and Red Sea, and potentially the Arabian Sea, include higher numbers than elsewhere in the world (Fig. 4). Also of interest is the absence of a relationship between CCL or clutch size and number of yolkless eggs (Table 4). Given the high nest temperatures experienced by eggs in the Gulf (Loughland 1999; SCENR 2006 in Pilcher et al. 2015; Al-Ghais 2009; Chatting et al. 2021), and predicted to occur in the Red Sea (Tanabe et al. 2020) and Arabian Sea (Willson et al. 2020), yolkless eggs in hawksbill turtle nests may fulfill roles proposed for leatherback turtles, including that of thermal buffering (Frazier and Salas 1984) and moisture reservoir (Hall 1990; Dutton and McDonald 1995; Wallace et al. 2006). This is a new area of consideration, because other studies of sea turtle responses to warming climates have focused on changes in geographic distribution, reproductive phenology, thermal reaction norms for sex determination, and maternal effects on offspring phenotype (see Maurer et al. 2021). The limited clutch count data available for other species in the northern Indian Ocean suggests that green sea turtles nesting in the Gulf may also lay large numbers of yolkless eggs (Al-Merghani et al. 2000; Al-Mohanna et al. 2014; Table 5), so the functional role and occurrence of yolkless eggs in different species throughout the region also needs to be examined more closely as a potential adaptation to extreme nest environments.

Table 5. Number of yolkless eggs laid by green turtles in the Persian Gulf and Red Sea. — = range is missing.

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Our findings suggest that the relatively small body and clutch sizes of hawksbill turtles nesting in the Gulf, Red Sea, and potentially Arabian Sea, are unique in comparison with other populations worldwide, and may be a response to poor foraging habitat and/or extreme aquatic environments, and the number of yolkless eggs are a potential adaptation to extreme nest environments. A better understanding of these relationships may provide insights into potential impacts of climate change on sea turtles and what adaptations might be beneficial.