Parasite diversity in sea turtles of the temperate SW Atlantic: a bridge between systematics and ecology

doi:10.21203/rs.3.rs-4600556/v1

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Parasite diversity in sea turtles of the temperate SW Atlantic: a bridge between systematics and ecology

https://doi.org/10.21203/rs.3.rs-4600556/v1

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Parasite studies can provide insights into important aspects of host ecology, which can be particularly important for species of conservation concern. This research focuses on the parasite diversity of two sea turtle species —the loggerhead Caretta caretta and leatherback Dermochelys coriacea sea turtles— in the temperate Southwest Atlantic, a region and species relatively understudied. Over a 15-year period (2008–2023), 30 sea turtles were sampled from the northern coast of Argentina. Through morphological and molecular tools, we identified five parasite species (the digeneans Pyelosomum renicapite and P. longiusculus, the nematodes Kathlania leptura and Sulcascaris sulcata and the leech Ozobranchus margoi) in loggerheads; and two digeneans (P. renicapite and O. amphiorchis) in leatherbacks. All species constitute the first report of the parasite in Argentina, and O. amphiorchis represents a new host-parasite association for leatherbacks. Comparative biogeographic analysis using the Regional Management Unit framework revealed that parasites could reveal connectivity between RMUs, though there are several information gaps. Increasing parasite studies can help understand sea turtle feeding ecology, ontogenetic shift and health status, and thus enhance conservation strategies for sea turtles globally.

loggerhead turtle

leatherback turtle

digenea

nematoda

Argentina

Parasite studies can provide insights into major threats to global biodiversity, such as overexploitation, habitat fragmentation, and climate change among others (Gagne et al. 2022). In aquatic environments, these studies offer valuable information on critical aspects of host ecology, including feeding habits, migrations, and exposure to environmental contaminants and stressors (Marcogliese 2004, 2023). Given the role of parasites in regulating host population (Marcogliese and Price 1997), such studies are particularly important for species of conservation concern.

Sea turtles are a group of seven species listed in categories from Data Deficient to Critically Endangered (IUCN 2023). For most species, the life cycle includes an ontogenetic shift from oceanic to neritic habitats, as well as a transition from omnivorous, pelagic feeding behavior to a more specialized, benthic feeding behavior (Musick and Limpus 1997; Bolten 2003). Even though most species connect ocean regions separated by thousands of kilometers, individuals often remain in certain feeding areas long enough to become infected with parasites (Greiner 2013). Sea turtle’s parasites have received considerable attention over time (e.g. Luhman 1935; Lester et al. 1980; Santoro et al. 2020), with greater focus on parasite systematics (Hamann et al. 2010) compared to ecological studies. While parasites are quite well known for certain turtle species and areas (e.g. the green turtle Chelonia mydas has the largest number of parasite records worldwide, much of which come from the Northwest Atlantic; Greiner 2013), there are regions and species for which parasitological knowledge is still limited.

Sea turtles are organized into Regional Management Units (RMUs) based on genetic stocks, geographic distribution, and migration patterns. RMUs delineate sea turtle assemblages below the species level but above the population level or breeding rookery. Within RMUs, sea turtles share demographic trajectories arising from similar biological and anthropogenic environmental factors (Wallace et al. 2010a, 2023). By integrating biogeographical information across life stages, RMUs provide a suitable framework for comparing several aspects of sea turtle populations, including natural history features, threats, and conservation status across the species global range (e.g. Fuentes et al. 2013; Wallace et al. 2010b, 2020; Esteban et al. 2020; Robinson and Pfaller 2022).

In this study, we explore the parasite diversity of two sea turtles species relatively underrepresented in parasite studies: the loggerhead (Caretta caretta) and leatherback (Dermochelys coriacea) turtles. Our focus is in the South West Atlantic (SWA) region (Fig. 1a), where the few existing parasite records are limited to tropical and subtropical areas (e.g. Werneck and Silva 2016), leaving a knowledge gap in southern temperate latitudes (> 34ºS). In fact, only one record of a parasite has been reported in this region more than 40 years ago (Boero and Led 1974). Specifically, we aim to: 1) identified the parasites present in loggerhead and leatherback turtles in the temperate SWA through morphological and molecular tools, and 2) to compare parasite diversity of both turtle species with that described in the rest of their global distribution using the RMUs framework. We discuss the implications of our findings for current knowledge on the connectivity between RMUs, feeding ecology of the species, and health status of populations. Additionally, we identify gaps and outline next steps in parasite studies on sea turtles.

Study area and specimen collection

Dead sea turtles were collected between December and May during the period 2008–2023 along more than 1,000 km of coastline of northern Argentina (Fig. 1a). Specimens were found stranded at beaches or recovered from bycatch in artisanal gillnets. Standard curved carapace length (SCL) was measured according to Bolten (2000) and ontogenetic stage was determined following the minimum size at the nearest nesting sites in the SWA, i.e., 83 cm for loggerheads and 139 cm for leatherbacks (Baptistotte et al. 2003; Thomé et al. 2007). Necropsy was performed on recently dead to moderately decomposed turtles following Work (2000). The digestive tract was extracted and separated into esophagus, stomach and intestine. Each section was opened longitudinally and the content was collected using water and a container. The contents were then filtered through two sieves, a large one of 10 mm mesh and a smaller one of 300 µm. Other viscera such as lung, liver, heart and kidney were also examined for parasites. The filtrate and the organs were separated into capsules to be examined under a stereoscopic microscope. Parasites found were preserved in ethanol 70% for their morphological identification. Some specimens were isolated in Eppendorf tubes and frozen at -20⁰C for genetic analysis.

Morphological and genetic study of parasites

For morphological identification of nematodes and hirudineans were temporarily mounted and cleared in Amman’s Lactophenol, and trematodes were stained with hydrochloric carmine, dehydrated in a graded ethanol series, cleared in eugenol, and permanently mounted in natural Canada balsam for their study using a polarizing microscope (Olympus BX51®, Tokyo, Japan). Additionally, photographs were taken with a Q-Imaging Go-3 digital camera. Specimens were identified according to Looss (1899), Werneck et al. (2012), and Greiner (2013). Prevalence (P), abundance (A) and mean intensity (MI) were calculated for each parasite species (Bush et al. 1997). Specimens were deposited in the Helminthological Collection of Museo de La Plata (La Plata, Buenos Aires province, Argentina- number requested).

For genetic characterization DNA was extracted from isolates using 200 µl of 5% Chelex solution (Bio-Rad Laboratories, CA, USA), 0.2 mg/ml Proteinase K (Roche) and incubated overnight at 56⁰C followed by 10 min at 95⁰C. Nuclear 18S, 28S, and ITS2 rDNA amplification were done using the appropriate primers (Littlewood, 1994; Cribb et al., 1998, Floyd et al., 2005). Each 50 µl PCR contained 25 µl of GoTaq Green Master Mix (Promega, Madison, Wi, USA) 2.5 µl of each primer, 17 µl of water, and 3 µl of extracted DNA. PCR amplification for 18S was performed using an Eppendorf Mastercycler ep gradient S, consisting of 94°C for 15 min, followed by 35 cycles of 94°C for 30 s, 60°C for 30 s, and 72°C for 70 s, with a final extension of 72°C for 240 s, for 28S amplification the program consisting of 94 ⁰C 4 min, followed by 30 cycles of 95 ⁰C for 60 s, 60 ⁰C for 60 s, and 72 ⁰C for 120 s, with a final extension of 72 ⁰C for 4 min, and for ITS2 amplification was one cycle of 95°C 3 min, 42°C 2 min and 72°C 1 min, followed by 6 cycles of 95°C 45 s, 47°C 45 s and 72°C 1 min, followed with 35 cycles of 95°C 20 s, 50°C 20 s and 72°C 1 min, and a final extension of 72°C for 5 min.

PCR products were purified and sequenced by Macrogen, South Korea. Sequences were edited and aligned using Chromas® version 2.6.6 and GAP® version 4.11.2 (Bonfield et al. 1995) and then compared with the NCBI database using BLAST version 2.2.26 (Altschul et al. 1997) to find sequences similar to those obtained.

Biogeographic analysis

To compare the parasite diversity of turtles from the temperate SWA with previous records in the rest of the region and the species global distribution we conducted a literature search by means of Google Scholar and PubMed. We searched the keywords "sea turtles", "Dermochelys coriacea", "leatherback", "Caretta caretta", "loggerhead", "parasites", "Nematoda", "Digenea", “Cestoda” and “Ozobranchus”. For each report found, we recorded the location and the parasite species, along with any information on its prevalence, intensity and abundance when available. The records found were then assigned to the 10 and seven RMUs defined by Wallace et al. (2023) for loggerheads and leatherbacks, respectively.

Turtle morphometrics

Loggerhead SCL ranged from 60.0 to 115.0 cm (mean = 70.9 ± 13.2 cm, n = 21), corresponding to juvenile and adult individuals. Leatherback SCL ranged from 133.0 to 155.0 cm (mean = 146.3 ± 8.6 cm, n = 6), corresponding to sub-adult and adult individuals.

New records of parasites in the temperate SWA

A total of 4505 parasite individuals were recovered and identified in 24 loggerhead (P = 83.3; A = 4407; MI = 1695) and six leatherback turtles (P = 83; A = 98; MI = 19.6). In loggerheads, parasite species found were Orchidasma amphiorchis (P = 33; A = 829; IM = 112.6), Pleurogonius longiusculus (P = 4; A = 1; IM = 1), Pyelosomum renicapite (P = 37; A = 557; IM = 61.8), Kathlania leptura (P = 20; A = 296; IM = 59), Sulcascaris sulcata (P = 79; A = 2277; IM = 119.8) and Ozobranchus margoi (P = 4; A = 447; IM = 447); while in leatherbacks only O. amphiorchis (P = 50; A = 15; IM = 5) and P. renicapite (P = 33; A = 83; IM = 41.5) were recorded (Fig. 1b). All parasites were found in the digestive tract, no individuals were found in the rest of the viscera.

The 18S gene sequence was obtained for the nematodes K. leptura and S. sulcata (GenBank acc. Num: XXXXX, GenBank acc. Num: XXXXX, respectively). While the sequence of K. leptura was the first molecular contribution, the sequence of S. sulcata aligned (99% similarity) with those previously recorded in GenBank and thus confirmed the morphological identification (Fig. 2). In addition, the 28S gene sequence for the digenean O. amphiorchis (GenBank acc. Num: XXXXXX), and the ITS2 gene sequence for the digenean P. renicapite (GenBank acc. Num: XXXXXX) from loggerheads, were obtained. Both records did not match any sequences in GenBank because there are no previous sequences available for these species.

Distribution of sea turtle parasites

We found 67 scientific papers reporting 58 parasite species for loggerheads and seven species for the leatherbacks worldwide (Figs. 3, 4, Tables 1, 2). Of the 10 loggerhead RMUs, the Northwest Atlantic (NWA) had the most parasite records (n = 34), followed by the Mediterranean (MED, n = 30), SWA (n = 17, of which five are new contributions resulting from the present work), and Southeast Indian (SEI, n = 12). The remaining RMUs had less than ten parasite records (Fig. 3; Table 1).

Table 2

Parasite species reported for *Dermochelys coriacea* by Regional Management Unit (RMU) defined by Wallace et al. (2023).
Species	RMU	Reference
Digenea
Calycodes anthos	Northwest Atlantic	Threlfall 1979; Innis et al. 2010
Calycodes anthos	Southwest Atlantic	Werneck et al. 2012
Cymatocarpus sp.	Northwest Atlantic	Threlfall 1979
Enodiotrema carettae		Manfredi et al. 1996
Enodiotrema instar		Manfredi et al. 1996
Enodiotrema sp.		Innis et al. 2010
Pyelosomum renicapite	Northeast Indian	Mohan 1970
	Northwest Atlantic	MacCallum 1921; Threlfall 1979; Almor et al. 1989; Dyer et al. 1995; Manfredi et al. 1996; Innis et al. 2010; Poppi et al. 2012
	Southwest Atlantic	Werneck et al. 2012; Present study
Orchiodasma amphiorchis	Southwest Atlantic	Present study

For leatherbacks, only three of the seven RMUs recorded parasites, with the NWA having the highest number of records (n = 6), followed by the SWA (n = 3, of which one is a new contribution from this work) and the Northeast Indian (NEI, n = 1) (Fig. 4; Table 2). Gaps of parasite records were identified in the Northwest and Southwest Indian for loggerheads; and in the Southwest Indian, and East and West Pacific RMUs for leatherbacks.

Loggerheads from the SWA shared parasite species with several other RMUs: 13 species with the NWA, 11 with the MED, 5 with the SEI and one with the NEI. However, two parasite species were exclusive found in the SWA: Monticellius indicum, and P. elongatus (Table 1). Of the parasites identified in this study, P. longiusculus was also documented in the NWA and NEI, O. margoi in the NWA and MED, O. amphiorchis, K. leptura and S. sulcata in the NWA, MED and SEI, and P. renicapite was recorded in the NWA and at the confluence of the NWA, MED and NEA. Similarly, leatherbacks from the SWA shared parasite species with the MED, NWA and NEI. Only O. amphiorchis was exclusive of the SWA.

In this study we provide new records of parasites for the loggerhead and leatherback turtles in the temperate SW Atlantic, region and species understudied. Particularly in Argentina, present study gives to known the second record of O. amphiorchis since it was found in a loggerhead by Boero and Led (1974). Also, new geographic records for loggerhead’s parasites including the digeneans P. longiusculus and P. renicapite, the nematodes K. leptura and S. sulcata, and the leech O. margoi are provided. We report P. renicapite in a leatherback for the first time in Argentina, and the finding of O. amphiorchis represents a new host-parasite association. Genetic information for K. leptura, O. amphiorchis and P. renicapite are given for the first time. Comparing on a global scale, the SWA share some parasite species with other RMUs in the northern and east hemispheres, but also exhibit exclusive parasite species. Gaps in parasite studies occur mostly in the East Atlantic, East Pacific and the Indian Ocean.

Parasite studies and the ecology of sea turtles

Mapping parasite diversity throughout sea turtle global distribution raises questions about many aspects of turtle ecology. One of these aspects is sea turtle migration and connectivity among RMUs. According to general parasitological knowledge, the biogeographic distribution of a parasite reflects that of its host (Marcogliese and Price 1997) to the extent that parasites are used as population biomarkers in several marine species (e.g. Catalano et al. 2014). Does the biogeographic distribution of turtle parasites resemble the biogeographic distribution of their hosts? More precisely, can sea turtle parasites be used to better resolve current RMUs? Founding the answers to these questions is not straightforward. For example, loggerheads from the SWA share parasite species with those of the NWA, in accordance with the partial overlap defined by Wallace et al. (2023) based on genetic and migration information (Fig. 3). But SWA loggerheads also share parasite species with more distant ࣧnot overlappingࣧ RMUs, such as the MED, NEI and SEI (see Table 1). Given that most parasitic infection in sea turtles requires the occurrence of an intermediate host (Corner et al. 2022; Santoro et al. 2022), the shared parasite species among distant but non-overlapping RMUs likely arise from similar ecological conditions in regions. This similarity allows for the independent development of the parasite life cycle, rather than from undocumented connectivity (through turtle migration) between RMUs.

At the same time, each loggerhead RMUs exhibit exclusive parasite species (e.g. M. indicum in the SWA, see Table S1 on Online Resource 1) that could act as biomarkers of turtles, especially in regions where RMUs overlap. For example, MED overlap with NWA and NEA (Fig. 3) particularly in the western Mediterranean. Cribb et al. (2017) distinguish between western and eastern Mediterranean turtles, highlighting that the former may bring their parasites from the NWA. Which is the origin of a loggerhead found in this region? If there was sufficient parasitological knowledge of turtles, this question could be answered relatively easy by examining common and exclusive parasite species (Fig. 5). Species such as Anisakis pegreffii and Styphlotrema solitaria have been recorded both in MED and at the overlap zone of the three mentioned RMUs but not in NWA, so a turtle harboring both parasite species might belong to MED rather than to the Atlantic. Inversely, species such as Rhadinorhynchus pristis has been documented only at the overlap zone of the three RMUs and not in the relatively well-studied MED and NWA, indicating that a loggerhead found in this region might belong to the NEA (where no parasite has been recorded yet). Similarly, parasites present in the overlap zone of the three RMUs and as well in MED and NWA, could be expected to be found in the unexplored NEA. Implementation of parasites as biomarkers of turtle origin requires an exhaustive sampling of turtle parasites throughout RMUs, to ensure that exclusive parasite species are not the product of insufficient number of hosts examined.

Parasites can also be useful in studies of feeding ecology. Most marine helminth parasites have intermediate hosts that depend on trophic interactions for their transmission (Marcogliese 2004, 2005), so the identification of a parasite species can be indicative of host diet, especially in regions where such information is scarce. In the SWA, nine studies list prey of loggerheads and leatherbacks (e.g. Frazier 1985; Carranza et al. 2010; DiBeneditto et al. 2015), but none of these prey were reported to be intermediate host for these turtles. Sulcascaris sulcata is the only sea turtle parasite for which the life cycle is known (Berry and Cannon 1981). This parasite has an indirect life cycle, with a bivalve or gastropod mollusc acting as intermediate host (Sprent 1977; Santoro et al. 2022). In this study, S. sulcata was recorded always associated with the presence of gastropods in the digestive tract of loggerheads (e.g. Rapana venosa, Pachycymbiola spp, Zidona spp.; Personal observation), but unfortunately its intermediate host could not be identified.

Another aspect that can be informed by parasite studies is the ontogenetic shift undergone by sea turtles within RMUs. In this study, the parasite prevalence in loggerhead was higher than that observed by Werneck et al. (2008) in Brazil (76% vs 41.7%). These authors recorded three digenean species (Calycodes anthos, O. amphiorchis and P. renicapite) and two nematode species (K. leptura and S. sulcata), with C. anthos as the dominant species. We recorded the same parasite species (except for C. anthos), but S. sulcata was the dominant species. While differences in prevalence could be due to the origin of the hosts, the Argentine ones coming from strandings and the Brazilian ones coming from fishing by-catch (Werneck et al. 2008), also, differences in parasite communities among regions may obey to ecological reasons. For example, in the Mediterranean, differences in parasite communities among regions and turtles reflect the ontogenetic shift that loggerheads undergo from oceanic to neritic habitats (Santoro et al. 2010). Small pelagic juveniles exhibit a less diverse parasite community (only conformed by E. megachondrus and C. anthos) compared to larger neritic juveniles, which parasite community includes several species of nematodes as well (Santoro et al. 2010a). In the SWA, more information on the size of loggerheads included in parasite studies is needed to evaluate if differences in parasite communities are informative of turtle ecology. Loggerheads analyzed in this study were large neritic juveniles and adults, but unfortunately information on turtle size provided by Werneck et al. (2008) is incomplete, thus limiting the scope of any comparison.

Lastly, parasite studies can be informative of the health status of turtle aggregations. We found a higher abundance of S. sulcata individuals (A = 2277) compared to that observed in other regions like Brazil (A = 33, Werneck et al. 2008) and Mediterranean (A = 196, Manfredi et al. 1998). Sulcascaris sulcata infection in loggerheads are known to be linked to ulcerative gastritis in the stomach mucosa. The severity of these lesions measured by the size of ulcers, correspond to the number of S. sulcata individuals (Santoro et al. 2019). In our study, we observed non-perforated ulcers (4 cm length) associated with S. sulcata in four out of the 24 turtles analysed. However, it is unlikely that parasitic infection contributes to the debilitation of the animals, since most of them exhibited good body condition, as evidenced by the presence of intracoelomic fat and recent food ingestion. On the other hand, the leech O. margoi found in this study is vector of the Chelonid Herpes Virus Type 5 (CHPHV-5) and other turtle-associated viruses (Rittenburg et al. 2021). Turtles infected with CHPHV-5 can develop fibropapillomatosis, characterized by the presence of internal and external benign tumors that, in severe cases, can lead to death due to wasting (Adnyana et al. 1997; Aguirre and Lutz 2004). While only one case of a green turtle with tumors was recently reported in Argentina (Origlia et al. 2023), fibropapillomatosis is frequent in the rest of the SWA (Silva-Junior et al. 2019). Considering the presence of O. margoi in loggerheads, virus infection could be expected even without the development of tumors (Gattamorta 2015). Therefore, studies to detect the virus in apparently uninfected turtles in Argentina would be necessary.

Limitations of parasite studies in sea turtles and next steps

Mapping parasite diversity throughout the RMUs of loggerheads and leatherbacks raises interesting question about host ecology, but also present some limitations. As noted by Poulin and Morand (2000), a key challenge in biogeographic studies of parasites is the risk that a map illustrating the distribution of species among regions merely reflects the variability in research activity among different parts of the world. In addition, from the non-studied RMUs, our estimation of parasite diversity in regions such as the Indian and the Pacific oceans is based on a few studies, examining less than five turtles. This suggests that several parasite species remain unrecorded due to an insufficient number of hosts examined. This is specially truth for leatherbacks, for which the limited parasite diversity observed can be attributed to the challenge of recovering and analysing hosts of considerable size (> 200 kg). Future parasite studies should prioritize understudied RMUs such as the NEA, the North and Southwest Indian, and the Pacific, for both loggerheads and leatherbacks. Additionally, comparisons of RMUs regarding the prevalence, intensity and abundances of parasites could not be performed in this study, given that these ecological parameters are rarely reported in both turtle species. Future parasite studies should also include these ecological data, along with precise information on the size of the turtles examined.

Particularly in the SWA, next steps should include the identification of intermediate hosts of turtle parasites to a better understanding of the trophic relationships. This is especially important for preys like gelatinous plankton, which is difficult to identify due its rapid digestibility (Arai 2005; Doyle et al. 2007). Sea turtles and their digeneans parasites offer a unique opportunity to assess long-term feeding relationships. These parasites exhibit high host specificity in both their intermediate and definitive hosts, especially when the final host is a reptile (Chabaud and Bain 1994). Further studies are essential to actively search for latent viruses in turtles and their possible vectors, as well as other pathogenic agents. A comprehensive health diagnosis of populations is crucial to developing effective conservation plans.

The contribution of new records of sea turtle parasites, both geographically and in terms of new parasite-host associations, represent a significant step towards a better understanding of turtle ecology. However, to enhance the utility of parasite studies in understanding turtle ecology, it is crucial to gather more information on the parasites of current and probable preys of turtles. This will help advance our knowledge on the biodiversity and structure of food webs that support sea turtles. In this work, we show how knowledge of a parasite species ecology, such as S. sulcata, can provide us with valuable information about sea turtles, including diet, ontogenetic, and health status. Furthermore, integrating the systematics of parasites with the existing knowledge from RMUs can facilitate the development of tools for predicting the RMUs of the turtles found and the parasite species present in unstudied regions. However, our knowledge of the global parasite diversity of loggerhead and leatherback turtles is still incomplete, with parasite studies lacking in several regions. We encourage for genetic characterization of parasites to help future research on phylogenetic relationships.

Author Contribution

E.O.P and V.G.C conceived and designed research. E.O.P, V.G.C, K.C.A, S.R.H, A.R, M.V, I.M.B, J.P.L, L.D and A.F carried out fieldwork. E.O.P, V.G.C, M.R.W and J.I.D analyzed data and wrote the manuscript. All authors read and approved the manuscript.

Acknowledgement

This manuscript would not be possible without the collaboration of artisanal fishers from San Clemente del Tuyú, who provided sea turtle individuals found dead in fishing gear. We are also grateful to technicians and researchers from Fundación Mundo Marino and Parque Educativo Mundo Marino, Prefectura Naval Argentina, park rangers and lifeguards from Buenos Aires province, who assisted during fieldwork. We also thank the support given by the Mar del Plata Aquarium thorough Alejandro Saubidet. Funding was partially provided by the Subsidio del Fondo para la Investigación Científica y Tecnológica (FONCyT) to the project Nº 1575-2017 of VGC. This is INIDEP contribution no. XXXX.

The authors have no relevant financial or nonfinancial interest to disclose.

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Table 1 is available in the Supplementary Files section.

No competing interests reported.

OnlineresourceTableS1.xlsx
Table 1S Parasite species reported for Caretta caretta by RMU.
Table1.xlsx
Table 1. Parasite species reported for Caretta caretta by Regional Management Unit (RMU) defined by Wallace et al. (2023). (External file)

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Parasite diversity in sea turtles of the temperate SW Atlantic: a bridge between systematics and ecology

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Abstract

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Introduction

Materials and methods

Study area and specimen collection

Morphological and genetic study of parasites

Biogeographic analysis

Results

Turtle morphometrics

New records of parasites in the temperate SWA

Distribution of sea turtle parasites

Discussion

Parasite studies and the ecology of sea turtles

Limitations of parasite studies in sea turtles and next steps

Conclusion

Declarations

Author Contribution

Acknowledgement

References

Table 1

Additional Declarations

Supplementary Files

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