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Ontogenetic diet shifts of green sea turtles (Chelonia mydas) in a mid-ocean developmental habitat

DOI:10.1007/s00227-018-3290-6
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Claire M. Burgett
Claire M. Burgett
Claire M. Burgett
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Derek A Burkholder at Nova Southeastern University
Derek A Burkholder
Kathryn Coates at Bermuda Government
Kathryn Coates
  • Bermuda Government
Virginia L. Fourqurean
Virginia L. Fourqurean
Virginia L. Fourqurean
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Abstract and Figures

Green sea turtles (Chelonia mydas) arrive on the geographically isolated Bermuda Platform as small juveniles and remain until they are approaching sexual maturity, at which point individuals depart for distant feeding and nesting sites. It has been reported that younger green turtles generally tend to carnivory or omnivory and that seagrasses become a significant food source as the turtles grow. Evidence indicates that grazing by green sea turtles in Bermuda is negatively impacting seagrass beds, thus understanding their diets is important to both conserving the turtles and their food. Stable isotope methods were used to investigate ontogenetic diet shifts of green sea turtles and to determine reliance on seagrass by larger turtles. Skin samples from 157 individual turtles and samples of known turtle foods, plants and animals, were collected for determination of consumer and food 13C and 15N values. A Bayesian stable isotope mixing model analysis indicated a wide range among individual turtles’ diets, with the greatest differences occurring between small and large turtles; larger turtles consumed seagrass almost exclusively. We also examined diet changes in 12 turtles captured in two successive years; these recapture data confirmed the changes in diet suggested by the relationship between size of turtles and diet composition. Very limited evidence was found of any diet variation among larger turtles that would indicate a shift away from declining seagrasses as their major food source.
Capture locations of turtles on the Bermuda Platform. Inset shows location of Bermuda in the western North Atlantic Ocean
Capture locations of turtles on the Bermuda Platform. Inset shows location of Bermuda in the western North Atlantic Ocean
… 
Nitrogen and carbon stable isotope ratios (in standard δ notation in ‰) for all green turtles (Chelonia mydas, n = 157) and potential food groups (macroalgae, n = 60; animals, n = 52; and seagrass, n = 455) on the Bermuda Platform. Descriptive box-and-whisker plots in the margins show the distribution of the values for each group, with median at the central line, first to third quartile in the boxes (IQR), and the whiskers indicate 1.5 × IQR. Open circles in the box-and-whiskers plots indicate data outside 1.5 × the IQR
Nitrogen and carbon stable isotope ratios (in standard δ notation in ‰) for all green turtles (Chelonia mydas, n = 157) and potential food groups (macroalgae, n = 60; animals, n = 52; and seagrass, n = 455) on the Bermuda Platform. Descriptive box-and-whisker plots in the margins show the distribution of the values for each group, with median at the central line, first to third quartile in the boxes (IQR), and the whiskers indicate 1.5 × IQR. Open circles in the box-and-whiskers plots indicate data outside 1.5 × the IQR
… 
Size distribution of the green sea turtles (Chelonia mydas) captured in 2012, given in the frequency of observations within 10 cm categories of SCL
Size distribution of the green sea turtles (Chelonia mydas) captured in 2012, given in the frequency of observations within 10 cm categories of SCL
… 
Variation in stable isotope ratios (A: δ¹³C, B: δ¹⁵N, in ‰) of skin samples as a function of size class for captured green turtles (Chelonia mydas). There were significant differences among size classes in δ¹³C [ANOVA, F (4, 152) = 35.6, P < 0.001], but no significant differences in δ¹⁵N [ANOVA, F (4, 152) = 1.6, P = 0.173]. Letters denote homogenous subsets of the data (Tukey post hoc test). N by size class: 20–30 cm = 28; 30–40 cm = 73; 40–50 cm = 29; 50–60 cm = 16; 60–70 cm = 11
Variation in stable isotope ratios (A: δ¹³C, B: δ¹⁵N, in ‰) of skin samples as a function of size class for captured green turtles (Chelonia mydas). There were significant differences among size classes in δ¹³C [ANOVA, F (4, 152) = 35.6, P < 0.001], but no significant differences in δ¹⁵N [ANOVA, F (4, 152) = 1.6, P = 0.173]. Letters denote homogenous subsets of the data (Tukey post hoc test). N by size class: 20–30 cm = 28; 30–40 cm = 73; 40–50 cm = 29; 50–60 cm = 16; 60–70 cm = 11
… 
a Absolute change in δ¹³C as a function of straight carapace length for all recaptured green turtles (Chelonia mydas) from Bermuda. b Absolute change in δ¹⁵N for as a function of straight carapace length for all recaptured turtles from Bermuda. Y-axes indicate difference in stable isotope ratios between years for each individual
+3
a Absolute change in δ¹³C as a function of straight carapace length for all recaptured green turtles (Chelonia mydas) from Bermuda. b Absolute change in δ¹⁵N for as a function of straight carapace length for all recaptured turtles from Bermuda. Y-axes indicate difference in stable isotope ratios between years for each individual
… 
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Vol.:(0123456789)
1 3
Marine Biology (2018) 165:33
https://doi.org/10.1007/s00227-018-3290-6
ORIGINAL PAPER
Ontogenetic diet shifts ofgreen sea turtles (Chelonia mydas)
inamid‑ocean developmental habitat
ClaireM.Burgett1· DerekA.Burkholder1,2 · KathrynA.Coates3· VirginiaL.Fourqurean4,5 ·
W.JudsonKenworthy6· SarahA.Manuel3· MarkE.Outerbridge3· JamesW.Fourqurean1
Received: 13 June 2017 / Accepted: 10 January 2018 / Published online: 19 January 2018
© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
Green sea turtles (Chelonia mydas) arrive on the geographically isolated Bermuda platform as small juveniles and remain
until they are approaching sexual maturity, at which point individuals depart for distant feeding and nesting sites. It has been
reported that younger green turtles generally tend to carnivory or omnivory and that seagrasses become a significant food
source as the turtles grow. Evidence indicates that grazing by green sea turtles in Bermuda is negatively impacting seagrass
beds, thus understanding their diets is important to both conserving the turtles and their food. Stable isotope methods were
used to investigate ontogenetic diet shifts of green sea turtles and to determine reliance on seagrass by larger turtles. Skin
samples from 157 individual turtles and samples of known turtle foods, plants and animals, were collected for determination
of consumer and food δ13C and δ15N values. A Bayesian stable isotope mixing model analysis indicated a wide range among
individual turtles’ diets, with the greatest differences occurring between small and large turtles; larger turtles consumed
seagrass almost exclusively. We also examined diet changes in 12 turtles captured in two successive years; these recapture
data confirmed the changes in diet suggested by the relationship between size of turtles and diet composition. Very limited
evidence was found of any diet variation among larger turtles that would indicate a shift away from declining seagrasses as
their major food source.
Introduction
Through their lives animals may experience profound
changes in ecology and biology, among these are fundamen-
tal changes in food sources and choices. Ontogenetic shifts
in diet are a common feature of the life history of a diverse
group of organisms, ranging from arthropods to vertebrates
(Werner and Gilliam 1984). Such shifts are frequently cou-
pled with changes in size and habitat. Ontogenetic shifts
from carnivorous and omnivorous juveniles to herbivorous
adults are common in reptiles, including green sea turtles
(Werner and Gilliam 1984; Polis etal. 1996). Stable isotope
diet studies have shown such a shift from a macroalgal and
animal-based diet in the pelagic environment of very young
green turtles to a plant-based diet after the juvenile turtles
move into neritic habitats (e.g., Reich etal. 2007; Arthur
etal. 2008; Howell etal. 2016).
The availability, quality and kinds of food in different
environments may vary widely, and animals must have
behaviors that ensure survival across all the conditions
encountered in their lifetime. Many marine organisms with
ontogenetic diet shifts have larvae and juveniles that feed
Responsible Editor: L. Avens.
Reviewed by Undisclosed experts.
Electronic supplementary material The online version of this
article (http s://doi.org/10.1007 /s002 27-018-3290 -6) contains
supplementary material, which is available to authorized users.
* James W. Fourqurean
jim.fourqurean@fiu.edu
1 Department ofBiological Sciences, Marine Education
andResearch Center, Florida International University,
OE148, 11200 SW 8th St, Miami, FL33199, USA
2 Present Address: Halmos College ofNatural Sciences
andOceanography, Nova Southeastern University, 8000
North Ocean Drive, DaniaBeach, FL33004, USA
3 Department ofEnvironment andNatural Resources, Bermuda
Ministry oftheEnvironment, HamiltonParishFL04,
Bermuda
4 Miami Palmetto Senior High School, 7460 SW 118th St,
Pinecrest, FL33156, USA
5 Present Address: Marine Education andResearch Center,
Florida International University, OE148, 11200 SW 8th St,
Miami, FL33199, USA
6 109 Holly Lane, Beaufort, NC28516, USA
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... During the oceanic juvenile life stage (< 30 cm curved carapace length, CCL), both green and hawksbill turtles consume omnivorous diets (Bolten 2003;Reich et al. 2007;Fukuoka et al. 2019). Subsequently, turtles recruit to coastal foraging habitats where diets begin to shift towards herbivory in green turtles and specialization on sponges in hawksbill turtles (Howell et al. 2016;Burgett et al. 2018;Ferreira et al. 2018). However, the degree of this shift is temporally and spatially specific (Bell 2013;González Carman et al. 2014;Santos et al. 2015;Tomaszewicz et al. 2018) and individualistic (Vander Zanden et al. 2013; Thomson et al. 2018). ...
... Thus far, stable isotope research in green and hawksbill sea turtles has been used in diet, niche and trophic modeling which has been beneficial in identifying alternative foraging strategies and dietary items Cardona et al. 2012;González Carman et al. 2014;Thomson et al. 2018;Méndez-Salgado et al. 2020;Gama et al. 2021;Seminoff et al. 2021). Further, these models inform on temporal dietary switching, from historical diets (Conrad et al. 2018) to ontogenetic shifts (Reich et al. 2007;Vander Zanden et al. 2013;Howell et al. 2016;Burgett et al. 2018;Ferreira et al. 2018) to annual or seasonal patterns (Páez-Rosas et al. 2021). Geographically, stable isotope analysis has allowed scientists to link diet and foraging to specific and sometimes undiscovered habitats important to sea turtles (Lemons et al. 2011;Bradshaw et al. 2017;Hancock et al. 2018;Tomaszewicz et al. 2018;Fukuoka et al. 2019;Piovano et al. 2020) in addition to relating diet to oceanographic parameters such as sea surface temperature (Esteban et al. 2020). ...
... Isotopically, we expect the juvenile habitat and dietary shift (Cherel and Hobson 2007;Seminoff et al. 2021) to be accompanied by an increase in δ 13 C values (shifting from oceanic to coastal isotope ratios; Cherel and Hobson 2007) and a decrease in δ 15 N values (shifting from omnivory/carnivory to herbivory; González Carman et al. 2014;Howell et al. 2016;Burgett et al. 2018;Ferreira et al. 2018). In other words, age-related ontogenetic shifts in diet predict that with increasing CCL, green and hawksbill turtle tissue should display an increase in δ 13 C values (similar to what we measured in black turtles) and a decrease in δ 15 N values. ...
Diet and foraging niche flexibility in green and hawksbill turtles
Article
Full-text available
We used stable isotopes to investigate isotopic niche size, overlap, and diet composition in green (black and yellow morphotype Chelonia mydas; 50.0 to 95.0 cm curved carapace length, CCL) and hawksbill turtles (Eretmochelys imbricata; 38.5 to 83.0 cm CCL) in a recently described foraging habitat in North Pacific Costa Rica. We measured whole blood stable carbon (δ¹³C) and nitrogen (δ¹⁵N) ratios in black (n = 39; mean ± SD, − 16.54 ± 0.66‰ and 14.39 ± 0.77‰), yellow (n = 13; − 15.74 ± 0.65‰ and 12.37 ± 0.55‰) and hawksbill turtles (n = 13; − 16.23 ± 1.34‰ and 12.63 ± 0.32‰) and skin δ¹³C and δ¹⁵N values in black (n = 36; − 15.32 ± 0.79‰ and 15.16 ± 0.72‰), yellow (n = 12; − 15.38 ± 0.91‰ and 13.78 ± 0.75‰) and hawksbill turtles (n = 10; − 14.33 ± 1.49‰ and 13.77 ± 0.29‰). Isotopic niche space revealed distinctly higher δ¹⁵N area in black turtles and significant overlap between yellow and hawksbill turtles, and a recent shift in diet in yellow turtles from omnivory to herbivory. In black turtles, isotopic niche suggests individual specialization during the non-upwelling season and generalization in diet during the upwelling season. Mixing model results suggest that black turtles forage at multiple trophic levels (fish: 34.8 ± 10.1% of diet and macroalgae: 51.8 ± 12.8% of diet), while yellow and hawksbill turtles primarily forage on macroalgae (85.0 ± 6.6% in yellow turtles and 85.1 ± 5.9% in hawksbill turtles). These results add to a growing understanding that diet in sea turtles is influenced by diet items present in the environment and suggest that black turtles are potential tertiary consumers.
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... "The point is made that many of the organisms of Bermuda are at or near the extreme poleward limit of their possible tolerance, that they have no margin to spare" (De Laubenfels 1950:158). about seagrass ecosystem decline and loss of ecosystem services (Lal et al. 2010;Scott et al. 2018), there is concern about how the loss of seagrasses might impact the ongoing recovery of green turtles that rely on seagrasses as a primary food source (Fourqurean et al. 2010;Christianen et al. 2014;Burgett et al. 2018;Gulick et al. 2020). Although there is ample data to suggest that green turtles can use alternative resources to seagrasses (Brand-Gardner et al. 1999;Lemons et al. 2011;Burgett et al. 2018;Esteban et al. 2020), significant decline in seagrass can be expected to produce changes in the demographics and ecology of herbivores that rely on them. ...
... about seagrass ecosystem decline and loss of ecosystem services (Lal et al. 2010;Scott et al. 2018), there is concern about how the loss of seagrasses might impact the ongoing recovery of green turtles that rely on seagrasses as a primary food source (Fourqurean et al. 2010;Christianen et al. 2014;Burgett et al. 2018;Gulick et al. 2020). Although there is ample data to suggest that green turtles can use alternative resources to seagrasses (Brand-Gardner et al. 1999;Lemons et al. 2011;Burgett et al. 2018;Esteban et al. 2020), significant decline in seagrass can be expected to produce changes in the demographics and ecology of herbivores that rely on them. The focus of this paper is a long-term study by the Bermuda Turtle Project (BTP) that documents significant demographic changes in a mixed-stock, developmental (non-adult) foraging aggregation of C. mydas at a site where seagrass declines (primarily Thalassia testudinum) have been documented (Murdoch et al. 2007;Fourqurean et al. 2010Fourqurean et al. , 2019Manuel et al. 2013;this study). ...
... The marked reduction in average size and mass of individual turtles is consistent with expectations drawn from a recent stable isotope (SI) study of green turtle diet done in conjunction with BTP sampling in 2012 and 2013 (Burgett et al. 2018). That study estimated that seagrass contribution to the tissues of green turtles varied from 5-80% (average 47%) with an ontogenetic shift to a more seagrass-focused diet at a size of ~ 40 cm. ...
A half-century of demographic changes in a green turtle (Chelonia mydas) foraging aggregation during an era of seagrass decline
Article
Full-text available
To understand the demographic responses of green turtles to seagrass decline, we examined a data set from study of a mixed-stock foraging aggregation of immature green turtles, Chelonia mydas, collected in Bermuda (32o18’N, − 64o46’W) over five decades. Average turtle size (SCLmin) and mass declined by 22.3% and 58.2%, respectively. Aggregation size structure shifted to smaller sizes and now consists of more small turtles and fewer large turtles. Density (turtles ha⁻¹) increased significantly but biomass (kg ha⁻¹) remained unchanged and low compared to C. mydas biomass observed elsewhere. Green turtles exhibited reduced site fidelity during two portions of the study period, suggesting increased foraging effort. Reduction in turtle body condition index and seagrass coverage occurred from offshore to inshore. Changes in aggregation composition and behavior were consistent with expectations given a documented decline in seagrass availability, combined with increased output from source rookeries. Apparent response to resource decline is traced back to 1976, well before seagrass loss was first documented. Green turtles and their primary food source (Thalassia testudinum) are at the northern limit of their range in Bermuda, where seagrasses would be expected to have a reduced tolerance for natural grazing pressure and increased susceptibility to synergistic stressors, especially temperature, bioturbation and phosphorus limitation. Our results suggest that synergistic stressors, and not green turtles alone, have produced the observed reduction in seagrasses on the Bermuda Platform. Given that seagrass declines have been reported worldwide, our findings may suggest how green turtles will respond elsewhere.
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... Variation in diet with body size has previously been reported in populations of C. mydas (e.g. Cardona et al. 2009;Morais et al. 2014;Howell et al. 2016;Burgett et al. 2018) and several lines of evidence described in our study suggest that size-related dietary variation also occurs for Ningaloo C. mydas. The increase in trophic position (TP) estimates with size based on δ 15 N AA values suggests that differences in bulk tissue δ 15 N values between size classes are due at least in part to differences in trophic level and cannot be explained entirely by differences in baseline δ 15 N values. ...
... This is in contrast to other populations where seagrass consumption increases with size (e.g. Cardona et al. 2010;Burgett et al. 2018), possibly due to differences in spatial and temporal availability of food resources and differences in habitat use. ...
... It appears that this substantial contribution from animal material reported in many green turtle populations (e.g. Hatase et al. 2006;Burkholder et al. 2011;Burgett et al. 2018;Fukuoka et al. 2019) also occurs in C. mydas foraging at Ningaloo. Jellyfish abundance in the lagoon at Ningaloo is temporally variable, and ephemeral (Ingram 2015) which meant that we were unable to collect samples. ...
Stable isotope composition of multiple tissues and individual amino acids reveals dietary variation among life stages in green turtles (Chelonia mydas) at Ningaloo Reef
Article
Full-text available
Diet is fundamental to an individual’s biology because energy acquired from food constrains growth and reproduction, which subsequently influences survival. It is, therefore, important to have a strong understanding of a population’s diet for species of conservation concern, such as the green turtle (Chelonia mydas). While the diet of adult green turtles is generally characterised as primarily herbivorous, growing evidence suggests variation in diet between and within populations is prevalent. We use complementary stable isotope analysis techniques to elucidate diet variation within a C. mydas population (ranging from small juveniles to adults) foraging at Ningaloo Reef in Western Australia. Analyses of multiple tissues and samples from ten individuals recaptured between 4 months and 4.5 years apart revealed that adults showed the highest levels of individual specialisation and consistency in diet over time. Analysis of red blood cell δ¹³C and δ¹⁵N values revealed macroalgae is likely the dominant food source for all size classes, and sub-adult and adults also ate animals (probably jellyfish). Compound-specific stable isotope analysis of amino acids indicated the main sources of essential amino acids for Ningaloo C. mydas were macroalgae or bacteria. Taken together, these results suggest C. mydas at Ningaloo conform to the general description of adult C. mydas diet as predominantly herbivorous, but diet varies with size and between adult individuals. Consideration of within-population diet variation will be important for predicting responses to stressors such as climate change, that directly affect foraging resources, as fitness consequences may vary for individuals with different diets.
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... SIA has been widely applied in trophic and dietary studies of marine megafauna (Boecklen, 2011;Haywood et al., 2019). In this group, observation of feeding events and assessment of foraging areas is often difficult or impossible and so, by analyzing the isotopic composition of tissue samples, it is possible to assess their trophic dynamics and cryptic lifestyles (Hatase et al., 2006;Vander Zanden et al., 2013;Burgett et al., 2018). The most common isotopes used in trophic studies are those of carbon and nitrogen (Lepoint et al., 2004;Boecklen, 2011) : stable carbon isotope ratios (d13C) are linked to the baseline sources of trophic webs, being useful to trace back the origins of consumed resources , while stable nitrogen isotope ratios (d15N) accumulate gradually along the food chain, being good indicators of the trophic level of a consumer (Deniro and Epstein, 1981). ...
... For green turtles (Chelonia mydas, Linnaeus, 1758), regarding foraging ecology alone, SIA has helped us uncover just how heterogenous their feeding habits can be (Esteban et al., 2020). Within populations, heterogeneity of foraging habits can range from ontogenetic differences in diet (Burgett et al., 2018), to unexpected pelagic feeding of previously thought obligate herbivore adults (Hatase et al., 2006), to sexspecific trophic variation (Roche et al., 2021). These differences can sometimes be significant within relatively small geographic scales, such as on the opposite shores of a single island (Hancock et al., 2018) or even within a single foraging area, diverging between individuals or age groups (Vander Zanden et al., 2013). ...
Fine-scale foraging segregation in a green turtle (Chelonia mydas) feeding ground in the Bijagós archipelago, Guinea Bissau
Article
Full-text available
  • Aug 2022
Green turtles ( Chelonia mydas ) are highly dependent on neritic foraging areas throughout much of their life. Still, knowledge of recruitment dynamics, foraging habits, and habitat use in these areas is limited. Here, we evaluated how the distribution and food preferences of green sea turtles from different life stages varied within a foraging aggregation. We focused on two islands in Guinea-Bissau, Unhocomo and Unhocomozinho, using water captures and survey dives to record habitat use and characteristics, and stable isotopes to infer diet. Additionally, we used stable isotopes to infer their diet. Two habitat types were sampled: deeper (2.26 ± 0.4 m) rocky sites fringed by mangrove with macroalgae, and sandy shallows (1.37 ± 0.12 m) surrounded by rocky reefs with macroalgae and seagrass. The two benthic communities were similar isotopically and in terms of species composition, except for the presence or absence of seagrass, which had unique signatures. We captured 89 turtles ranging from 35 cm to 97 cm in curved carapace length (i.e., juvenile to adult stages). Size distribution was habitat-dependent, with most smaller turtles present in sandy shallows and larger turtles favoring slightly deeper rocky sites. Turtle isotopic signatures differed between the habitat of capture, regardless of size, revealing a marked dichotomy in foraging preference. All turtles fed primarily on macroalgae, mostly rhodophytes. However, individuals captured in sandy habitats had evident seagrass skewed isotopic signatures. Larger turtles may be unable to use the more diverse shallower foraging sites due to increased vulnerability to predation. Despite the proximity of the sampled foraging sites (2.7 km apart), the two foraging subgroups seem to maintain consistently different feeding habits. Our study highlights how heterogeneous green turtle foraging habits can be within populations, even at small geographic scales.
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... Green turtles display an ontogenetic shift in diet toward herbivory at sizes greater than 30 cm CCL in benthic habitats (Burgett et al., 2018) and have a predominantly seagrass-based diet in the Western Indian Ocean (Stokes et al., 2019). For example, juvenile green turtles forage on animal matter in coastal habitats of southern Peru and then transition from a high-to low-calorie diet when they migrate north to feed on abundant vegetation (Quiñones et al., 2022). ...
Synergistic use of UAV surveys, satellite tracking data, and mark-recapture to estimate abundance of elusive species
Article
  • Mar 2023
Estimating population abundance is central to many ecological studies and important in conservation planning. Yet the elusive nature of many species makes estimating their abundance challenging. Abundance estimates of sea turtles , marine birds, and seals are usually made when breeding adults are ashore, while life stages spent at sea, including as juveniles, are often poorly sampled. We used a combination of high-resolution satellite tracking (Fastloc-GPS), uncrewed aerial vehicle (UAV) surveys, and capture-mark-recapture approaches to assess the abundance of immature hawksbill (Eretmochelys imbricata) and green turtles (Chelonia mydas) in a tidal lagoon of the Chagos Archipelago (Indian Ocean). We captured, marked, and released 50 turtles (48 hawksbill and 2 green turtles) prior to UAV surveys and used satellite tracking data from 27 immature turtles (25 hawksbill and 2 green turtles) to refine the estimated numbers of marked turtles available for resighting and those likely to have emigrated from the study area. We estimated a total of 339 turtles in the lagoon with a density variation at different tidal heights between 265 turtles km −2 at high water and 499 turtles km −2 at low water. Of these, 91% were hawksbills and 9% were green turtles. These hawksbill densities are the highest reported among 17 foraging sites recorded around the world and likely reflect successful long-term protection of turtles in the Chagos Archipelago.
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... Green turtle diets differ according to their life stage, geographic zones and ranges. Generally, green turtles are omnivorous during the early pelagic stages and then become primarily herbivorous after recruitment to the neritic zone (e.g., Reich et al., 2007;Howell et al., 2016;Vélez-Rubio et al., 2016;Burgett et al., 2018). In addition to diet, the levels of metals observed in sea turtle tissues may also depend on the environmental quality of their surrounding environment, which is often altered by human activities. ...
Metal accumulation in juvenile and sub-adult loggerhead and green turtles in northern Cyprus
Article
Sea turtles are considered pollution bioindicators due to their tendency to accumulate high metal levels in their tissues during their long lifespans. In this context, we aimed to analyse the concentrations of 12 elements in liver, kidney, heart and muscle samples from green turtles (Chelonia mydas; n = 41) and loggerhead turtles (Caretta caretta; n = 14) found stranded in Northern Cyprus. The samples were collected between 2019 and 2021, stored in sterile Eppendorf tubes at −20 °C until metal analysis, and analysed with an inductively coupled plasma mass spectrometer. With this study, we contribute to the limited number of studies on metal accumulation in heart tissue and present the first data for Mg accumulation in the heart, liver, muscle and kidney tissues of both species. We found that metal accumulation levels differed among the two study species’ tissues, with some elements in the same tissue (AlKidney, AsHeart, AsLiver, FeMuscle, FeKidney, FeHeart, MnHeart, PbHeart, ZnMuscle and ZnKidney) significantly differing between species. The observed variation likely resulted from their different feeding habits, which cause them to be exposed to different levels of metals. We also found significant associations among elements within tissues, as well as between the same element across different tissues in both species, which may indicate the differential accumulation of elements among organs due to physiological processes in turtle metabolism, bioaccumulation or excretion.
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... Stable isotope approach in chelonian research has been primarily used on sea turtles (e.g., Petitet and Bugoni, 2017;Burgett et al., 2018;Figgener et al., 2019;Pearson et al., 2019), with a growing application to freshwater populations (e.g., Seminoff et al., 2007;Lara et al., 2012;Pearson et al., 2013;Balzani et al., 2016). In this study, we used stable isotope analyses to quantify isotopic signatures of P. gorzugi and determine the extent of niche overlap of P. gorzugi and T. scripta across different habitats in the Pecos River tributaries. ...
Using Stable Isotopes to Study Resource Partitioning between Red-eared Slider and Rio Grande Cooter in the Pecos River Watershed
Article
Full-text available
  • Feb 2022
Aquatic turtles represent important biotic components of freshwater ecosystems. The Pecos River watershed is inhabited by six freshwater turtle species, including the widespread Trachemys scripta (Red-eared Slider) and a species of conservation concern, Pseudemys gorzugi (Rio Grande Cooter). Here, we assessed isotopic niche widths of Rio Grande Cooter and niche overlap where it co-occurs with Red-eared Slider in the Pecos River tributaries, New Mexico, USA. We used carbon (d 13 C) and nitrogen (d 15 N) stable isotope analyses of two different tissue types: blood and claw. Our results showed niche partitioning among different populations of P. gorzugi and among sex classes within a population. At the sites where both species occur, we documented niche overlap, especially for d 15 N values. Stable isotopes showed similar ellipse area overlap (SEA B) of T. scripta and P. gorzugi among populations (~20% 2), but little to no overlap of standard ellipse areas for small sample sizes (SEA C). The distribution of prey items in the diets of P. gorzugi and T. scripta revealed the differences in resource selection. We observed that differences in the diets of P. gorzugi among populations correspond to local resource availability, suggesting opportunistic foraging behavior of P. gorzugi. Our study aids in understanding the ecology and natural history of P. gorzugi, one of the least studied freshwater turtles in the USA. Moreover, our study provides insights to interspecific relations of T. scripta in their native range.
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... The inter-island movements also indicate that once Thalassia seagrass declines in Kalpeni, green turtles may move to another seagrass-rich lagoon within the Lakshadweep islands or to another nearby site rich in their preferred seagrasses in case there is no shift in their dietary choice (see Burgett et al. 2018). Habitatdriven shifts in herbivores have been seen in Shark Bay, Ningaloo and Exmouth Gulf, where the loss in available forage resulted in dugongs moving to a different region (Gales et al. 2004). ...
The island hoppers: how foraging influences green turtle (Chelonia mydas) abundance over space and time in the Lakshadweep Archipelago, India
Article
Full-text available
  • May 2022
Adult green turtles are known to display either preference in their foraging habits or fidelity to their foraging sites which, in turn, influences their migrations and the availability of forage. With an abundant supply of seagrass and algae, the lagoons of the Lakshadweep Archipelago off the Indian west coast serve as significant feeding grounds for green turtles. In the last 2 decades, the numbers of foraging green turtles have varied across islands, leading to speculation about their foraging patterns and movements. We collated secondary data and conducted periodic surveys between 2013 and 2019 to record trends in green turtle abundance and seagrass characteristics and investigate relationships between them. Over the last decade, green turtle abundances have fluctuated widely with increases followed by sharp declines within different lagoons. Our results also show that a reduction in seagrass density, particularly Thalassia sp. and Cymodocea sp., coincided with the decline in green turtle abundance. Moreover, turtle presence was observed at sites with higher seagrass density and canopy height. Our findings indicate that green turtles appeared to forage in particular lagoons until their preferred resources declined, before moving to other islands within the Archipelago or other unknown locations. Therefore, to devise effective management strategies, it is crucial to understand how this green turtle population will adapt to the decline in foraging resources. The declining seagrass populations also suggest the need for an ecosystem approach towards green turtle conservation.
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Fibropapillomatosis infection in a population of green turtles at Watamu Bay, Kenya
Article
  • Aug 2021
Anthropogenic stressors from onshore and offshore activities can act as driving factors of disease for a wide range of marine organisms. Green turtles (Chelonia mydas) are prominently afflicted with a tumour-causing disease known as fibropapillomatosis (FP) caused by the chelonid alphaherpesvirus ChHV5. Previous studies indicate that pathways of FP transmission may be genetic (vertical transmission) or linked to causal factors in a turtle’s environment (horizontal transmission). In this paper patterns of FP prevalence were examined in 10,896 records of green turtles caught or found stranded around Watamu Bay, Kenya, between 2003 – 2020. Findings were focused on locational and seasonal factors that may potentially influence infection. The findings show that FP prevalence varies significantly on an annual basis. Location significantly influenced infection prevalence, with prevalence higher in open ocean sites than sites located within the creek. Infection prevalence was highest at sites around the creek mouth and north of the creek mouth, with both regions exhibiting disparate annual patterns of infection. This paper is the first to examine long-term trends of FP prevalence in-depth in this region and has implications for the health of turtles and marine biota found along the Kenyan coast, and potentially within the wider Western Indian Ocean region. The findings emphasize the need to distinguish the infection pathways of causative agents via: i) further examination of the links between infection and environmental and/or biont community factors; and ii) the collection of data pertinent to the genetic diversity of green turtles and associated ChHV5 viral strains occurring in the Western Indian Ocean.
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Impact of the socioeconomic activities on sea turtle conservation in the Potiguar Basin, north-eastern Brazil (2010–2019)
Article
Brazil has a coast that is threatened by economic activities and accelerated urbanisation process, causing ecosystem unbalance and decreasing socioenvironmental quality. We analysed data collected from 2010 to 2019 during the Beach Monitoring Project in north-eastern Brazil to quantify sea turtle strandings with signs of anthropogenic interaction, verify the impact of economic activities on the strandings, and analyse a possible relation between socioeconomic conditions and the strandings. Anthropogenic interaction was classified into 12 categories (eight related to fishing activities). We analysed 6007 strandings, including four sea turtle species and anthropogenic interaction was observed in 12.88% (n = 774) of the strandings. Chelonia mydas represented 94.05% of the total records with anthropogenic interaction and fishing-related strandings accounted for 81.65%. Juvenile individuals were more affected than adults; likewise, females were more affected than males. Icapuí and Areia Branca are very populous municipalities, and showed large number of strandings with signs of anthropogenic interaction. Our analyses revealed that fishing-related strandings were reported throughout the year; however, a larger number of records occurred in the dry season and during the lobster-fishing season. Our study brings knowledge on sea turtle strandings in north-eastern Brazil, providing results that support public policies to mitigate anthropogenic impacts on sea turtles.
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Long-term and seasonal patterns of sea turtle home ranges in warm coastal foraging habitats: Implications for conservation
Article
Full-text available
  • Dec 2016
Home range analysis is a powerful tool for identifying priority areas for conservation, but estimating the home range for many species is still challenging. In particular, highly mobile species may use different areas at different times (e.g. summer or winter), so temporally-biased location data may only partially represent their home range. We investigated the temporal patterns in habitat use of green turtles Chelonia mydas (n = 52) and loggerhead turtles Caretta caretta (n = 20) at longer (>1 yr) and shorter (<1 yr) scales. The study was conducted in subtropical and tropical foraging habitats along the Queensland coast of Australia between 1991 and 2015. Each turtle was tracked by a satellite-linked tag for the effective life of the device; three turtles were tracked twice. Mark-recapture studies were also conducted intermittently. Single satellite-tag deployments confirmed site fidelity to a foraging habitat for up to 2.5 yr by green turtles and 2.7 yr by loggerhead turtles. Further, combining satellite telemetry and mark-recapture records indicated much longer periods of foraging residency, up to 17 yr for green turtles and 23 yr for loggerhead turtles. No tracked turtles made substantial changes in their foraging range between years. Within the long-term home range, subtropical turtles tended to shift their foraging areas seasonally. Consequently, for many turtles, the existing conservation legislation provided protection in some seasons but not others. Our results emphasise the importance of protecting areas according to the turtles’ use of space, with careful consideration given to identify temporal trends in their habitat selection.
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Ontogenetic shifts in diet and habitat of juvenile green sea turtles in the northwestern Gulf of Mexico
Article
Full-text available
  • Nov 2016
Effective management of a rapidly increasing juvenile green sea turtle Cheloni mydas population necessitates an understanding of the foraging grounds utilized throughou ontogeny. We used stomach content (SCA) and stable isotope analyses (SIA) of multiple siz classes of green turtles foraging along the middle (MTC) and lower Texas coasts (LTC) in th northwestern Gulf of Mexico to identify ontogenetic shifts in foraging behavior. Spatial difference in diet and habitat residency were examined based on samples gathered from live (n = 55 and deceased turtles (n = 114). Additionally, the isotopic composition of putative forage materia within nearshore and inshore habitats was investigated to determine prey contribution to diet Green turtle recruitment to neritic channel environments in Texas waters at sizes 25 cm straigh carapace length (SCL) was established based on the presence of benthic macroalgae in the diet Integration of SCA with SIA of carbon and nitrogen in scute material, as well as potential prey revealed a subsequent inshore shift to seagrass beds before obtaining 35 cm SCL for turtles of th LTC, while turtles from the MTC exhibited considerable variation in size at transition. This stud improves our understanding of the feeding ecology of green turtles within critical foragin grounds along the Texas coast.
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Water quality, isoscapes and stoichioscapes of seagrasses indicate general P limitation and unique N cycling in shallow water benthos of Bermuda
Article
Full-text available
  • Oct 2015
  • BG
Striking spatial patterns in stable isotope ratios (isoscapes) and elemental ratios (stoichioscapes) of seagrass leaves and the water column nutrients indicate general P limitation of both water column and benthic primary productivity on the Bermuda Platform, and they highlight the role of the Bermuda Islands as a source of N and P. We found consistent differences among the four seagrass species (Syringodium filiforme, Thalassia testudinum, Halodule sp. and Halophila decipiens) in the N, P, d13C and d15N of leaf tissues. The d15N of seagrass leaves was especially variable, with values from -10.1 to 8.8 ‰, greatly expanding the reported range of values for all seagrass species globally. Spatial patterns from both the water column and the seagrass leaves indicated that P availability was higher near shore, and d15N values suggest this was likely a result of human waste disposal. Spatially contiguous areas of extremely depleted seagrass 15N suggest unique N sources and cycling compared to other seagrass-dominated environments. Seagrass N: P values were not as far from the stoichiometric balance between N and P availability as in the water column, and there were no strong relationships between the water column N: P and the seagrass N: P. Such isoscapes and stoichioscapes provide valuable ecogeochemical tools to infer ecosystem processes as well as provide information that can inform food web and animal movement studies.
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Increased use of non-native algae species in the diet of the Green Turtle (Chelonia mydas) in a primary pasture ecosystem in Hawaii
Article
Full-text available
  • Jul 2015
The Green Turtle, Chelonia mydas, has modified its feeding behavior over the past 36 years to include the increasing abundance of non-native algae growing in the greater Kaneohe Bay area of Oahu, Hawaii. Changes in diet of the Turtles are correlated with an increase in abundance of non-native algae. Turtles are eating 135 species of marine vegetation including the following seven non-native species: Acanthophora spicifera, Hypnea musciformis, Gracilaria salicornia, Eucheuma denticulatum, Gracilaria tikvahiae, Kappaphycus striatum and Kappaphycus alvarezii. Non-native algae now represent 0.64 proportion of the Turtle diet. The present study for the additional 8 years 2005–2012, shows the utilization of non-native species for food has increased 24% since the last study that included 28 years 1976–2005. Average time for the Turtles to make the shift to non-native species is 10–12 years for the more invasive species and 20–30 years for the slower growing species. During this same time period the numbers of C. mydas, body size, and growth rates have also increased, partly due to the increased abundance of the additional non-native food items. This study verifies that the trend of Turtles eating higher amounts of non-native algae in Kaneohe Bay is now stronger than first reported in 2009.
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Regional and local factors determining green turtle Chelonia mydas foraging relationship with the environment
Article
  • Jun 2015
Changes in green turtle Chelonia mydas foraging patterns were evaluated within a latitudinal gradient along tropical and subtropical coasts in the southwestern Atlantic and investigated as to how green turtles responded to regional and local changes in their foraging habitats. In addition, we evaluated how changes in feeding ecology caused populations to be more susceptible to various anthropogenic threats. The literature and original diet data of 427 green turtles were analyzed. Turtles from tropical and subtropical reefs exhibited the classic pattern of herbivorous benthic foraging, turtles from estuarine areas exhibited a more generalist diet and pelagic foraging, and turtles from colder reef areas, located between the winter isotherms of 10°C and 20°C, exhibited an omnivorous diet and pelagic foraging strategy. The amount of ingested animal matter was higher in occurrence and abundance in the green turtle diets in the most southern foraging areas. Foraging ecology was influenced by regional (phycogeographical provinces and water temperature) and local (urbanization and rivers) factors. Green turtles exhibited high foraging plasticity, and their importance to the ecosystem was not restricted to their role as herbivores. Green turtles may also have an important role as second-order consumers in certain areas, mainly in the cooler waters at the extremes of their distribution. Foraging plasticity was observed both in the type of diet item and foraging strategy, which implies that there may be variation in the exposure of populations to threats.
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Movements and Feeding Ecology of Immature Green Turtles (Chelonia mydas) in a Florida Lagoon
Article
The seasonal and diel movements of 14 green turtles (Chelonia mydas) in Mosquito Lagoon, Florida were monitored using sonic telemetry. The feeding ecology of this population was also studied using dissection and stomach flushing techniques. Immature green turtles made random, long distance movements (x̄ = 8.2 km/day) and occupied deeper waters (x̄ = 1.6 m), apparently not feeding, when water temperatures ranged from 11-18 C; at water temperatures above 25 C they adopted a home range. Turtles were active at temperatures up to 34 C. No diel pattern was evident during winter months, but a definite bimodal pattern was evident at high water temperatures, with green turtles feeding on grass flats in midmorning and midafternoon and moving into deeper waters during the midday hours. Home range area was significantly correlated with body weight but the center of grazing activity was not. Seagrasses made up 88% of the turtles' diet throughout the year.
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Nutritional Ecology of Sea Turtles
Article
Analysis of the nutritional ecology of sea turtles, that is, how nutrition influences their biology and determines their interactions with the environment, is necessarily restricted to the green turtle, Chelonia mydas. Our knowledge of the nutrition of the other species of sea turtles is limited to information on diet from gut content studies and a few reports on the anatomy and histology of the digestive tract. The literature on diet and gut anatomy and histology are summarized in the first two sections of this review. The remainder of this review is a discussion of the nutrition of Caribbean green turtles; their digestive efficiencies, adaptations to their major food plant Thalassia testudinum, and the effect the diet has, through nutrient limitation, on their productivity. Although Thalassia is a very abundant food source which is fairly constant in productivity and nutrient quality, few herbivores graze on it. Green turtles have two adaptations that enable them to utilize Thalassia more efficiently. First, they maintain grazing plots where, by cropping the young regrowth, they obtain blades of much higher quality because of lower lignin and higher nitrogen concentrations. Secondly, they have a hindgut microbial fermentation that digests the fiber in Thalassia and yields both an important energy source to the green turtle, in the form of volatile fatty acids, and gives the green turtle access to the highly digestible cell contents. In spite of the advantages of these adaptations-grazing plots and hindgut fermentation-they are not sufficient to prevent nutrient limitation and the resulting slow growth rates, delayed sexual maturity, and reduced reproductive output. Comparison with green turtles on high-quality, pelleted diets shows that the productivity of wild populations is well below their genetic potential. Ironically, nutrient limitation acting through delayed sexual maturity may benefit green turtles during periods of intense exploitation by man.
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