José Carlos Báez1,2*- 1Instituto Español de Oceanografía (CSIC), Centro Oceanográfico de Málaga, Fuengirola, Spain
- 2Instituto Iberoamericano de Desarrollo Sostenible (IIDS), Universidad Autónoma de Chile, Temuco, Región de la Araucanía, Chile
Sporadic sea turtle nesting within the western Mediterranean Sea
The loggerhead turtle, a predominant species in the Mediterranean Sea (DiMatteo et al., 2022), exhibits a diverse migratory behavior throughout its life history, with females showing a strong tendency toward philopatry during the nesting period (Omeyer et al., 2021); returning to the same locations where they were born. There is thus a convergence of individuals from eastern Mediterranean and Atlantic nesting areas in the western Mediterranean (Camiñas and de la Serna, 1995; Monzón-Argüello et al., 2010; Carreras et al., 2011; Camiñas et al., 2021).
In recent years there has been an unprecedented surge in nesting activities outside the traditional eastern Mediterranean nesting grounds. This unexpected occurrence of sporadic nesting events in the western Mediterranean has prompted hypotheses that it might signify an early stage of colonization (Carreras et al., 2018; Hochscheid et al., 2022). Despite the surge in nesting outside established areas, albeit one not extensively documented currently, recent genetic studies have revealed past instances of colonization (Santidrián Tomillo et al., 2023). Present climatic conditions in the western Mediterranean basin, though comparatively cooler than their eastern counterparts, have proven conducive for nesting (Santidrián Tomillo et al., 2023). In fact, medium and long-term forecasting models suggest the suitability of the western Mediterranean as a climatic refuge for loggerhead sea turtles (Witt et al., 2010; Pike, 2014). The empirical evidence suggests that sea turtle individuals nesting along the Spanish coast originate from distant populations in the Atlantic and eastern Mediterranean regions (Carreras et al., 2018; Luna-Ortiz et al., 2024), underscoring the occurrence of a long-range colonization process. Furthermore, the absence of remigrant individuals implies that nesting females are likely colonizers rather than residents (Luna-Ortiz et al., 2024). These findings have important implications for the conservation of loggerhead turtles, highlighting a notable expansion of nesting range from east to west within the Mediterranean basin (Mancino et al., 2022). Additionally, there has been a shift from a nesting window previously viable only in exceptional years to one now viable annually (Cardona et al., 2023). In this context, several authors have postulated that the observed behavioral alterations reflected in the heightened occurrence of sporadic sea turtle nesting within the western Mediterranean Sea might be attributed to climate change (Carreras et al., 2018; Hochscheid et al., 2022; Santidrián Tomillo et al., 2023).
The increase in sporadic loggerhead sea turtle nests could also be attributed to the rising density of loggerhead turtles in the Mediterranean. Despite the global threatened status of loggerhead turtles, conservation policies in the Mediterranean have led to its designation as a species of least concern on the IUCN Red List since 2015. Due to mounting pressures from tourism and rising temperatures, an increase in loggerhead sea turtles in the Mediterranean could lead turtles in the region to seek new nesting beaches.
The particular case of Alboran Sea
The Alboran Sea is a marine bridge that connects the Mediterranean and the Atlantic sea turtle populations. According to many studies based on stranding and by-catch data, loggerhead sea turtles from Atlantic nesting beaches migrate to the Mediterranean Sea through the Alboran Sea during the spring and summer seasons, while returning to the Atlantic Ocean during the winter season (Camiñas and de la Serna, 1995; Báez et al., 2011, Báez et al., 2017; Bellido et al., 2018). Moreover, Revelles et al. (2007) propose the presence of a permeable barrier within the Strait of Gibraltar which influences the dispersal patterns of juvenile loggerhead sea turtles. Consequently, juveniles originating from the Atlantic are unable to traverse the inward surface current, compelling them to reside in the Mediterranean until they attain a minimum size to overcome the flow of Atlantic waters. The delineation of the Alboran Sea is contingent upon the presence of distinct geographical boundaries flanking its longitudinal expanse, principally embodied by the Strait of Gibraltar and the hydrographic interface spanning from Oran to Cape Gata. These demarcations not only serve as geographical confines but also exert a discernible influence on species distribution, effectively demarcating the confines of a biogeographical domain. The easternmost sector is characterized by the Alboran Sea Frontal System. Under optimal conditions, the easternmost extension of this frontal system spans from Cape Gata to Oran, Algeria. However, this barrier may experience attenuation, permitting a restricted flux of species. Consequently, the Alboran Sea’s boundary exhibits permeability, with the eastern expanse of the province of Almería being attributable to the Alboran Sea in function to oceanography context at a moment (Vargas-Yáñez et al., 2002; Real et al., 2021; Vargas-Yáñez et al., 2021).
It is of interest that although the first loggerhead turtle nesting site detected in the Iberian Peninsula was found on the Andalusian coast (Tomás et al., 2002; Báez et al., 2021a), located proximate to the Alboran Sea border (in a broader biogeographical context, it might be considered part of the Alboran Sea), and despite the rise of sporadic nesting phenomena across the western Mediterranean, only four instances of loggerhead turtle nestings have been documented in or in close proximity to the Alboran Sea: Vera (Almería) on July 27, 2001; Pulpi (Almería) on July 17, 2015; Fuengirola (Málaga) on August 4, 2020; and Marbella (Málaga) on July 8 and Mojacar (Almería) on 29 August 2023 (Figure 1). There are no records of such nesting sites on the coast of Morocco (Báez et al., 2021a).
Figure 1 Location of the four sporadic nesting sites from the Alboran Sea and nearby areas. Key: V, Vera (Almería) on July 27, 2001; P, Pulpi (Almería) on July 17, 2015; F, Fuengirola (Málaga) on August 4, 2020; M, Marbella (Málaga) on July 8, and Mo, Mojacar (Almería) on 29 August, 2023. *Loggerhead sea turtle nesting activity location.
The Alboran Sea represents the viable threshold for loggerhead turtle nesting, with conducive climatic conditions being essential for nesting occurrences. To validate this proposition, it becomes imperative to establish a correlation between sporadic nestings and short-term climatic indices. Such an association would provide crucial insights into the potential impact of immediate climatic variables on the irregular nesting events observed, thereby strengthening the hypothesis of climate change’s influence on sea turtle nesting behavior within the Alboran Sea.
North Atlantic oscillation a short-term climate index affecting on sea turtles
The North Atlantic Oscillation (NAO) stands as the preeminent large-scale climatic fluctuation, exerting influence over the North Atlantic region in short-term periods. Its variability significantly impacts diverse meteorological parameters encompassing wind speed, direction, disparities in air temperature, and precipitation, notably during the boreal winter. Beyond its atmospheric effects, the NAO extends its influence to the ocean, instigating alterations in heat distribution, sea surface temperature, gyre circulation, mixed layer depth, salinity levels, high-latitude deep water formation, and sea ice coverage (reviewed in Báez et al., 2021b). Consequently, the NAO has garnered extensive attention in the analysis of marine ecosystems’ variability. Various studies have established a teleconnection between NAO fluctuations and migration of sea turtles through the Alboran Sea (Báez et al., 2011; Báez et al., 2017; Bellido et al., 2018).
The North Atlantic Oscillation (NAO) assumes positive and negative values, each eliciting distinct meteorological repercussions. The positive phase of the NAO induces above-average westerly winds across the northern mid-latitudes and fosters arid climatic conditions in the Mediterranean region whereas the negative phase leads to substantial precipitation in southern Europe. Beyond the directional implications of the NAO on storms and the qualitative meteorological conditions within the North Atlantic, the quantitative magnitude of this oscillation holds significant importance (reviewed in Báez et al., 2021b). Employing a binary logistic regression (using the software SPSS 17.0) to correlate the presence by year (i.e. 2001, 2015, 2020 and 2023 corresponding to the nests of Vera, Pulpí, Fuengirola and Marbella/Mojacar, respectively) or absence (i.e. 19 years without nests detected in or around the Alboran Sea) of nests with the observed mean July NAO for each year yields a statistically significant function (Omnibus Test= 5.252; df= 1; P= 0.022; Nagelkerk R2 = 0.338; AUC= 0.803). Therefore, despite the limited number of nests within the Alboran Sea region, evidence supports a causal relationship between loggerhead sea turtle nestings in the Alboran Sea and the state of the North Atlantic Oscillation.
Discussion
Over the nesting of 23 years, ranging from the initial recorded turtle nest in Vera 2001 to the most recent one in 2023, there is a prevalence of 14 years characterized by a mean negative North Atlantic Oscillation (NAO) during the month of July, while 9 years exhibit a mean positive July NAO. Notably, all four instances of turtle nestings occurred during years featuring a mean negative July NAO. Three specific occurrences, the Pulpi nesting in 2015 and the most recent in Marbella and Mojacar in 2023, align precisely with the years showcasing the most extreme negative July NAO values. NAO in negative phase favours the sporadic laying of loggerhead turtles in the Alboran Sea. Báez et al. (2013) found that the negative NAO could help to increase sea surface temperature from Alboran Sea.
Sea turtle are threat rising sea levels drive by climate change and severe storms under climate change, potentially diminishing available nesting beaches crucial for egg laying by sea turtles (Maneja et al., 2021). In addition, sea turtles exhibit temperature-dependent sex determination raising the possibility that climate-induced temperature increases could influence sex ratios in these populations (Tezak et al., 2020). Therefore, climate change may impact the ecology of sea turtles, as elucidated above, where the extremely negative North Atlantic Oscillation (NAO) in July could directly influence this process. Climate change is a global phenomenon on a broad scale, yet there is limited evidence of cases akin to the rise in sporadic nesting outside the western Mediterranean. A citizen science project indicated that despite Peru not being considered to have nesting beaches, at least two species were observed nesting and on the rise (Zavala and Kelez, 2015). However, this instance might stem from inadequate beach surveys rather than a shift in sea turtle behavior. Consequently, the absence of similar occurrences outside the Mediterranean might suggest the involvement of additional factors beyond climate change. However, the NAO is very sensitive to climate change, with periods of predominantly negative NAO, and more extreme oscillations (Báez et al., 2013). Therefore, the phenomenon of sporadic nesting on the beaches of the Alboran Sea will increase over time.
Author contributions
JB: Writing – original draft, Writing – review & editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study has been funded by the subproject ALMA within project “Design, validation and implementation of a monitoring network for the implementation of a network for monitoring biodiversity and ecosystem services in ecosystem services in anthropised environments in Andalusia”, in the framework of the complementary plan on biodiversity, financed by the recovery and resilience mechanism UE, and coordinated under the agreement between the “Concejería de Universidad, Investigación e Innovación de la Junta de Andalucía” and University of Pablo De Olavide on behalf of a group of participants entities.
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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References
Báez J. C., Bellido J. J., Ferri-Yáñez F., Castillo J. J., Martín J. J., Mons J. L. (2011). The North Atlantic Oscillation and Sea Surface Temperature affect loggerhead abundance around the Strait of Gibraltar. Sci. Mar. 75, 571–575. doi: 10.3989/scimar.2011.75n3571
Báez J. C., Gimeno L., Gómez-Gesteira M., Ferri-Yáñez F., Real R. (2013). Combined effects of the North Atlantic oscillation and the arctic oscillation on sea surface temperature in the Alborán sea. PloS One 8, e62201. doi: 10.1371/journal.pone.0062201
Báez J. C., Gimeno L., Real R. (2021b). North Atlantic Oscillation and fisheries management during global climate change. Rev. Fish. Biol. Fish. 31, 319–336. doi: 10.1007/s11160-021-09645-z
Báez J. C., Macías D., Bellido J. J., Camiñas J. A. (2017). Differential temporal and spatial distribution of adult loggerhead sea turtles from Gulf of Cádiz to western Mediterranean Sea. Vie Milieu. 67, 1–5.
Báez J. C., Macías D., García-Barcelona S., Poisson F., Torreblanca E., Bellido J. J., et al. (2021a). “Marine megafauna and charismatic vertebrate species,” in Alboran Sea, Ecosystems and Marine Resources. Eds. Báez J. C., Vázquez J. T., Camiñas J. A., Idrissi M. M. (Springer Nature, Gewerbestrasse, Switzerland), 712–753, ISBN: 978-3-030-65516-7. doi: 10.1007/978-3-030-65516-7
Bellido J. J., Torreblanca E., Báez J. C., Camiñas J. A. (2018). Sea turtles in the eastern margin of the North Atlantic: the northern Ibero-Moroccan Gulf as an important neritic area for sea turtles. Mediterr. Mar. Sci. 19, 662–672. doi: 10.12681/mms.15835
Camiñas J. A., de la Serna J. M. (1995). “The loggerhead distribution in the western Mediterranean Sea as deduced from captures by the Spanish longline fishery,” in Scientia Herpetologica. Eds. Llorente G. A., Montori A., Santos X., Carretero M. A. (Asociación Herpetológica Española, Barcelona), 316–323.
Camiñas J. A., Domingo A., Coelho R., Bruyn P., Abascal F. J., Báez J. C. (2021). Tuna regional fisheries management organizations and the conservation of sea turtles: A reply to Godley et al. Oryx 55, 12. doi: 10.1017/S0030605320000708
Cardona L., San Martín J., Benito L., Tomás J., Abella E., Eymar J., et al. (2023). Global warming facilitates the nesting of the loggerhead turtle on the Mediterranean coast of Spain. Anim. Conserv. 26, 365–380. doi: 10.1111/acv.12828
Carreras C., Pascual M., Cardona L., Marco A., Bellido J. J., Castillo J. J., et al. (2011). Living together but remaining apart: Atlantic and Mediterranean loggerhead sea turtles (Caretta caretta) in shared feeding grounds. J. Heredity 102, 666–677. doi: 10.1093/jhered/esr089
Carreras C., Pascual M., Tomás J., Marco A., Hochscheid S., Castillo J. J., et al. (2018). Sporadic nesting reveals long distance colonization in the philopatric loggerhead sea turtle (Caretta caretta). Sci. Rep. 8, 1435. doi: 10.1038/s41598-018-19887-w
DiMatteo A., Cañadas A., Roberts J., Sparks L., Panigada S., Boisseau O. (2022). Basin-wide estimates of loggerhead turtle abundance in the Mediterranean Sea derived from line transect surveys. Front. Mar. Sci. 9. doi: 10.3389/fmars.2022.930412
Hochscheid S., Maffucci F., Abella E., Bradai M. N., Camedda A., Carreras C. (2022). Nesting range expansion of loggerhead turtles in the Mediterranean: Phenology, spatial distribution, and conservation implications. Glob. Ecol. Conserv. 38, e02194. doi: 10.1016/j.gecco.2022.e02194
Luna-Ortiz A., Marín-Capuz G., Abella E., Crespo-Picazo J. C., Escribano F., Félix G., et al (2024). New colonisers drive the increase of the emerging loggerhead turtle nesting in Western Mediterranean. Sci. Rep. 14, 1506. doi: 10.1038/s41598-024-51664-w
Mancino C., Canestrelli D., Maiorano L. (2022). Going west: range expansion for loggerhead sea turtles in the Mediterranean Sea under climate change. Glob. Ecol. Conserv. 38, e02264. doi: 10.1016/j.gecco.2022.e02264
Maneja R., Miller J. D., Li W., Rejoice T., El-Askary H., Perera S. (2021). Multidecadal analysis of beach loss at the major offshore sea turtle nesting islands in the Northern Arabian Gulf. Ecol. Indic. 121, 107146. doi: 10.1016/j.ecolind.2020.107146
Monzón-Argüello C., Rico C., Naro-Maciel E., Varo-Cruz N., López P., Marco A., et al. (2010). Population structure and conservation implications for the loggerhead sea turtle of the Cape Verde Islands, Conserv. Genet 11, 1871–1884. doi: 10.1007/s10592-010-0079-7
Omeyer L. C. M., Stokes K. L., Beton D., Çiçek B. A., Davey S., Fuller W. J. (2021). Investigating differences in population recovery rates of two sympatrically nesting sea turtle species. Anim. Conserv. 24, 832–846. doi: 10.1111/acv.12689
Pike D. A. (2014). Forecasting the viability of sea turtle eggs in a warming world. Glob. Change Biol. 20, 7–15. doi: 10.1111/gcb.12397
Real R., Gofas S., Altamirano M., Salas C., Báez J. C., Camiñas J. A., et al. (2021). “Biogeographical and macroecological context of the Alboran Sea,” in Alboran Sea, Ecosystems and Marine Resources. Eds. Báez J. C., Vázquez J. T., Camiñas J. A., Idrissi M. M. (Springer Nature, Gewerbestrasse, Switzerland), 431–458, ISBN: 978-3-030-65516-7. doi: 10.1007/978-3-030-65516-7
Revelles M., Carreras C., Cardona L., Marco A., Bentivegna F., Castillo J. J., et al. (2007). Evidence for an asymmetrical size exchange of loggerhead sea turtles between the Mediterranean and the Atlantic through the Straits of Gibraltar. J. Exp. Mar. Biol. Ecol. 349, 261–271. doi: 10.1016/j.jembe.2007.05.018
Santidrián Tomillo P., Pujol F., Félix G., Núñez-Reyes V., Saba V., Tomás J., et al. (2023). Colonization of new nesting areas could provide climate refuge to loggerhead turtles under climate change. Biol. Conserv. 284), 110146. doi: 10.1016/j.biocon.2023.110146
Tezak B., Sifuentes-Romero I., Milton S., Wyneken J. (2020). Identifying sex of neonate turtles with temperature-dependent sex determination via small blood samples. Sci. Rep. 10, 5012. doi: 10.1038/s41598-020-61984-2
Tomás J., Mons J. L., Martín J., Bellido López J. J., Castillo J. (2002). Study of the first reported nest of loggerhead sea turtle, Caretta caretta, in the Spanish Mediterranean coast. J. Mar. Biolog. Assoc. UK. 82, 1005–1007. doi: 10.1017/S0025315402006537
Vargas-Yáñez, García-Martínez M. C., Moya F., Balbín R., López-Jurado J. L. (2021). “The oceanographic and climatic context,” in Alboran Sea, Ecosystems and Marine Resources. Eds. Báez J. C., Vázquez J. T., Camiñas J. A., Idrissi M. M. (Springer Nature, Gewerbestrasse, Switzerland), 85–110, ISBN: 978-3-030-65516-7. doi: 10.1007/978-3-030-65516-7
Vargas-Yáñez M., Plaza F., Lafuente J., Sarhan T., Vargas J. M., Velez-Belchi P. (2002). About the seasonal variability of the Alboran Sea circulation. J. Mar. Syst. 35, 229–248. doi: 10.1016/S0924-7963(02)00128-8
Witt M. J., Hawkes L. A., Godfrey M. H., Godley B. J., Broderick A. C. (2010). Predicting the impacts of climate change on a globally distributed species: The case of the loggerhead turtle. J. Exp. Biol. 213, 901–911. doi: 10.1242/jeb.038133
Keywords: climate change, NAO, Mediterranean Sea, sea turtle, nesting activities
Citation: Báez JC (2024) Is climate change modifying the behavior of sea turtles? The particular case of the loggerhead turtle in the Alboran Sea. Front. Mar. Sci. 11:1379303. doi: 10.3389/fmars.2024.1379303
Received: 30 January 2024; Accepted: 25 March 2024;
Published: 03 April 2024.
Edited by:
Todd Atwood, U.S. Geological Survey, Alaska, United StatesReviewed by:
Carlos Carreras, University of Barcelona, SpainCopyright © 2024 Báez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: José Carlos Báez, josecarlos.baez@ieo.csic.es