In the present study, ontogenetic shifts in the diet and habitat use of olive ridley sea turtles in northeastern Brazil were elucidated. Each sample from each LAG was considered an integration of information from throughout that given year, thus reflecting the “averaged” diet and habitat based on stable isotope values for that time interval. Therefore, the analysis of sequential LAGs should detect potential shifts in δ13C and δ15N values across interval of one-year long (Avens et al. 2013, 2020). We found that there is an ontogenetic shift at approximately 17 years of age, which is within the estimated range of age at sexual maturity (ASM) for this population (Petitet et al. 2015).
Young adults experience a wider range of habitats than do older adults, while there is a slight difference in trophic position between age groups, which suggests that younger individuals occupied the broadest niche, as shown by the greater variation in carbon than in nitrogen values. This interpretation indicates that older adults are more consistent over time in habitats used than are young adults, which is in line with the high variation in δ13C values for younger adults and with the observation of lower WIC values for δ13C in older adults than in young adults (WIC = 0.82 and 1.11, respectively). The youngest turtles could be in a phase when they learn where they have to go to forage and develop, thus consequently visiting more habitats than old adults do, and may ingest a variety of food items they find (Snover et al. 2007). Subadult olive ridleys from the Mexican Central Pacific population appear to use oceanic waters, as indicated by the carbon values in epidermal tissue (Carpena-Catoira et al. 2022). In other vertebrate groups, juveniles are also less selective in feeding than adults because they have to grow fast to minimize predation risk (Snover et al. 2007). Although isotopic nitrogen varied more with age than carbon did, there were small variations among individual trajectories, which suggests that older animals are slightly more consistent in resource use than younger animals. However, the nitrogen WIC values for both groups (young and older adults) indicated consistency in trophic position over the years sampled (0.71 and 0.56, respectively). The explanation for this pattern is related to the age group to which they belong; all animals sampled were in the adult phase, and some were sexually mature (Silva et al. 2007; Petitet et al. 2015). As expected, they invest in prey with high nutritional values, directed towards the energetic cost of reproduction, unlike juvenile turtles that invest in growth (Araújo et al. 2011). Moreover, a consistency in δ13C values seems to be established from 17 years old onwards, when they mature (Petitet et al. 2015). ASM is the time when olive ridley turtles migrate to coastal waters to mate and nest (Plotkin 2010); thus, recruitment to the breeding population seems to be accompanied by changes in diet and habitat after spending the entire immature phase in oceanic waters. However, the life cycle of olive ridley sea turtles is more complex because after nesting, they show variation in migratory strategies, as reported in Santos et al. (2019) with satellite telemetry of the same population examined in this study. These researchers demonstrated that some turtles move to feeding areas in northern Brazil and others migrate to feed in the southeast, while other individuals move to oceanic waters towards the west coast of Africa (Mauritania, Senegal, Guinea Bissau, Guinea and Sierra Leone) (Silva et al. 2011; Santos et al. 2019), which makes it difficult to infer the habitat use of this species. This species has the same complex life cycle in the eastern Pacific Ocean (Morreale et al. 2007; Plotkin 2010; Guzman et al. 2019). These studies corroborate the high variation in δ13C values found, as each sample is an average of the entire year, and could explain the high degree of individual variation among younger individuals, which was reflected in high BIC-to-TNW ratio values (~ 62%). Moreover, the wide range of habitats at different latitudes experienced by the olive ridley sea turtle population from northeastern Brazil could potentially explain the high variation in δ13C values, as well as the δ13C values from the epidermal tissue of loggerhead sea turtles sampled at various latitudes in the northern Atlantic Ocean (Pajuelo et al. 2012). On the other hand, there was no significant variation in carbon from plasma and red blood cells of the loggerhead sea turtle population in North Carolina or from epidermal tissue of the olive ridley sea turtle population in the Mexican Central Pacific sampled at similar latitudes, between neritic and oceanic waters (McClellan et al. 2010; Carpena-Catoira et al. 2022), which reinforces the influence of latitude on carbon values. Therefore, the temporal consistency shown by the older adults probably results from the accumulated experience of finding the best feeding areas every year, after and between nesting seasons, demonstrating that older individuals are more specialist than younger individuals.
The high interindividual variation among younger and smaller individuals is consistent with tracking data (Santos et al. 2019), which has demonstrated that the largest and intermediate-sized turtles migrate to southern and northern Brazil, respectively, while smaller turtles migrate to oceanic waters. This is also in line with the enrichment of δ15N with age demonstrated in the oldest individuals, as this group migrates to feeding areas with high primary productivity from the upwelling southeast of Brazil and discharge of the Amazon River in northern Brazil. Moreover, this migration pattern has also been detected in nesting and inter-nesting olive ridley females in French Guiana and Indonesia (Chambault et al. 2016; Fukuoka et al. 2022). Beyond the constancy in trophic position, the Brazilian population demonstrated high interindividual variation in nitrogen, explained by a high percentage of BIC within TNW for both groups (68% and 60%), which corroborates tracking data and the diverse feeding grounds of this species with differences in prey items.
The isotopic niche of older adults was narrower than that of young adults, which was reflected in TNW values for carbon (1.33 and 3.01, respectively) and nitrogen (1.43 and 2.26, respectively). The level of individual specialization indicated by δ15N values was higher than that for δ13C. Although young adults had slightly higher levels of individual specialization as indicated by δ13C than did older individuals, the level of individual specialization indicated by δ15N was similar for both groups (0.32 and 0.40). Even after recruitment, they may not change trophic level if isotopic values at the food web baseline are similar, as expected given homogeneous isoscapes in northeastern Brazil (McMahon et al. 2013). Green and adult loggerhead sea turtles studied by Vander Zanden et al. (2013) and Pajuelo et al. (2016) also had similar levels of specialization for δ15N, but δ13C seems to indicate higher specialization than found for olive ridley sea turtles in the current study. Notwithstanding, adult loggerhead and green sea turtles forage mostly near the coast, while olive ridley sea turtles forage in oceanic waters in addition to neritic foraging grounds (Silva et al. 2011; Santos el al. 2019). These are two marine realms with contrasting δ13C values, with wide variation in latitude (McClellan et al. 2010; McMahon et al. 2013), where turtles migrate along 30 degrees of latitude (Santos et al. 2019). Therefore, the area of overlap by the young group of the older group’s niche is ~ 56%, as their niche is wider than the niche of the oldest turtles.
SIMM also demonstrated differences in habitats used between young and older adults. Gelatinous prey made a major contribution to the diet of young individuals, most likely because they had been in oceanic waters in previous years (Santos et al. 2019). Although some older individuals also showed major contributions from jellyfish, the greatest contribution on average for the entire group was crustacean prey. Older adults, most likely mature individuals, may forage in neritic areas and eventually travel to areas off the continental shelf, which is narrow in northeastern Brazil. Colman et al. (2014) demonstrated that demersal fish and crustaceans had great importance in olive ridley diets in the study area, based mainly on dead stranded adults. All older individuals who showed jellyfish prey contributions also displayed, at similar values, crustacean prey contributions, while the oldest individuals exhibited major contributions from crustacean prey. Furthermore, these latter turtles were from the older adult group, ranged in age from 20 and 23 years old and were probably mature sea turtles (Petitet et al. 2015). Moreover, the 5 mature females were in this group, with jellyfish and crustacean prey contributions together or crustacean prey contributions alone predominating. This result is consistent with that for mature individuals, which demonstrated a major contribution from jellyfish in scute tissues (Petitet and Bugoni 2017), which reflects, in ectotherms, the diet and location from an earlier time period. Thus, the crustacean contribution found in mixed models may be from mature turtles that had migrated to neritic foraging grounds after nesting and stayed there until the next nesting season based on the migration pattern of the largest turtles in the same area (Santos et al. 2019). This scenario was demonstrated from the same population with serum tissue analysis of nesting olive ridley sea turtles, reflecting a major contribution from demersal fish and prey with high nutritional value such as crustaceans (Petitet and Bugoni 2017). Moreover, olive ridley females from French Guiana and Indonesia dove for food, from which it was deduced that they were feeding at the bottom (Chambault et al. 2016; Fukuoka et al. 2022), probably on demersal prey items as inferred from the oldest individuals in this study.
Post-nesting migration patterns generate high levels of interindividual variation in nitrogen values in both age groups, as corroborated by the low WIC/TNW ratio values of this stable isotope. However, for carbon values, the young adults had higher interindividual variation, which corroborated the low WIC/TNW ratio, while older adults had low variation between individuals and low within-individual variation. This could be masked by the high WIC/TNW ratio values in the oldest individuals (Vanden Zanden et al. 2013). Santos et al. (2019) showed that the largest individuals migrate to southeastern and northern Brazil; thus, together with lower WIC and lower BIC values for this group and with the analysis of individual trajectories of isotopic lines, older adults had a moderate degree of individual specialization for carbon. Therefore, in both groups, the WIC/TNW ratios for δ13C and δ15N were closer to 0, rather than 1, suggesting a moderate level of individual specialization (Bolnick et al. 2002). Due to high variability in migration patterns among individual adult olive ridley sea turtles (Silva et al. 2011; Santos et al. 2019), they seem to specialize eventually because they migrate to different habitats with different resources available. Moreover, migration to varied areas may decrease intraspecific competition, increasing individual specialization due to low densities (Araújo et al. 2011). In addition, olive ridley sea turtles from coastal India and the eastern Pacific Ocean have also been classified as generalist populations based on studies of diet and stable isotopes (δ15N and δ13C) from epidermal tissue, respectively (Behera et al. 2014; Peavey et al. 2017). The current study adds novelty regarding individual specialization over time based on sequential samples from individuals.