What makes marine turtles go: A review of metabolic rates and their consequences

doi:10.1016/j.jembe.2007.12.023

Journal of Experimental Marine Biology and Ecology

Volume 356, Issues 1–2, 3 March 2008, Pages 8-24

https://doi.org/10.1016/j.jembe.2007.12.023 Get rights and content

Abstract

Quantification of metabolic rates (MR) is fundamental to understanding an individual organism's physiology and life history, as well as overall population dynamics. Applications of MR measurements have increased both in quantity and quality across animal ecology over the past 50 years. Included in this trend, research on MRs of marine turtles and its consequences for these unique ectothermic vertebrates has matured significantly. We reviewed existing literature on marine turtle MRs in the context of the physiology, ecology, and life history of these animals. Metabolic rates have been obtained and published for 4 of 7 marine turtle species, but not for all life stages for all of these species. Studies of marine turtle metabolism have ranged from straightforward MR measurements of a few individuals to use of innovative techniques to estimate energy expenditure of natural activities and for applications to marine turtle energetics and diving physiology. Comparisons of allometric relationships between resting MR (RMR) and body mass for leatherbacks (Dermochelys coriacea), green turtles (Chelonia mydas), other reptiles, and mammals revealed no differences between leatherbacks and green turtles, nor between those species and other reptiles, but significant differences with mammals. In addition, we synthesized research on the thermal biology of the leatherback turtle, which ranges from temperate to tropical waters, and concluded that leatherbacks achieve and maintain substantial differentials between body and ambient temperatures in varied thermal environments through an integrated balance of adaptations for heat production (e.g., adjustments of MR) and retention. Finally, we recommend that future research should 1) address remaining data gaps in current knowledge of MRs of some species, 2) apply MR measurements to important physiological, ecological, and conservation topics, 3) investigate cellular metabolism of marine turtles, and 4) focus on quantification of at-sea energy expenditure incurred by marine turtles during natural activities.

Section snippets

Understanding The Fire of Life

Animal metabolism has long been considered The Fire of Life (Kleiber, 1961), a suite of processes unequivocally fundamental to an organism's individual physiology, life history, and survival, and thus to overall population-level processes. During the past half-century, developments in metabolism research have dramatically improved understanding of animal physiology and ecology. These developments have included novel and enhanced metabolic rate measurements, elucidation of the factors that

Overview of methods to obtain metabolic rates

Several methods have been used to obtain MRs in studies of animal physiology in general and marine turtles in particular. In this section, we present descriptions of these methods, their associated advantages and disadvantages, and studies that have employed them to measure or estimate marine turtle MRs (see Table 1 for summary).

Comparison of MRs among species and life stages

Measurements of marine turtle MRs obtained by various methods have been reported for several species and for different life stages (Table 2). Metabolic studies have been conducted and published on four species of hatchlings (loggerhead Caretta caretta, green, olive ridley, and leatherback turtles), two species of juveniles (loggerheads, greens), and two species of adults (greens, leatherbacks). To our knowledge, no published MRs exist whatsoever for flatback turtles (Natator depressus),

Applications of MR measurements to marine turtle ecology

While MR data are valuable by themselves, applications of MRs to broader, multi-faceted questions increase the relevance and importance of MR data to the study of marine turtle ecology and conservation. Metabolic rates – particularly at-sea MRs – for marine turtles are the most critical components in calculating individual and population energy requirements, improving our understanding of physiological limitations on diving and thermoregulation, and for refinement of demographic parameters

Future directions

While obtaining MR data for marine turtles is not always straightforward, the data themselves have great potential for important applications to physiology and conservation of these animals. Thus, despite the impressive body of research on marine turtle metabolism, there are several areas that still deserve attention. First, we propose that measuring MRs for species for which no MR data exist (Table 2) should be a priority. Second, where MR data exist, we recommend maximizing their potential

Acknowledgments

We acknowledge J. Davenport, D. Jackson, D. Jones, M. Lutcavage, P. Lutz, F. Paladino, H. Prange, and J. Spotila for their seminal contributions to marine turtle physiology research. We are also grateful to G. Hays and S. Shumway for organizing this marine turtle special issue. Thanks to J. Wyneken and A. Southwood for providing information from their respective studies that we included in this review, and to D. Jones for allowing T.T.J. to pursue this review as well as for monetary support

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Identifying dispersal pathways and critical habitats is essential to evaluate risks and inform effective management strategies of migratory marine species during all life stages. This is especially true for sea turtles that are conservation-dependent and for which management needs usually precedes comprehensive data collection. The aim of this study was to model dispersal pathways (representative of individual behaviour) and compare potential dispersal corridors (representative of population-level behaviour) of hawksbill, loggerhead, leatherback, and green sea turtles from key rookeries in the Western Indian Ocean (WIO) with different dispersal strategies. We used the Sea Turtle Active Movement Model (STAMM) to simulate post-hatchling dispersal under the combined effects of ocean currents and habitat-driven movements. Simulation results confirmed the high connectivity between hatching sites and developmental areas in the WIO; dispersal is mostly driven by ocean currents but differs among species and years with habitat quality also differing among species. Active swimming appeared to have little influence on their dispersal patterns during the first year. We then analysed simulation results using a movement-based kernel density estimation to identify dispersal corridors for each species. There were three distinct dispersal corridors: among equatorial Indian Ocean Islands (hawksbills); along East Africa (green turtles); and around southern Africa (loggerheads and leatherbacks). These results provide a first estimation of the dispersal pathways used by neonate turtles, that are usually lacking in conservation assessments. The results can also assist to develop more targeted management measures like RMU designation or marine spatial planning for the lost years.
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Sea turtles generally lay several clutches of eggs in a single nesting season. While a negative correlation between water temperatures and the time required between constitutive nesting events (termed the internesting interval) has been previously reported in loggerhead Caretta caretta and green turtles Chelonia mydas, it is not understood whether this relationship remains constant across other sea turtle species. Here, we expanded upon these previous studies on loggerhead and green turtles by using larger sample sizes and including data from species with a wider range of body-sizes; specifically: hawksbill Eretmochelys imbricata, leatherback Dermochelys coriacea, and olive ridley turtles Lepidochelys olivacea. In total, we compiled temperature data from biologgers deployed over internesting intervals on 23 loggerhead, 22 green, 7 hawksbill, 26 leatherback and 11 olive ridley turtles from nesting sites in 8 different countries. The relationship between the duration of the internesting interval and water temperatures in green and loggerhead turtles were statistically similar yet it differed between all other turtle species. Specifically, hawksbill turtles had much longer internesting intervals than green or loggerhead turtles even after controlling for temperature. In addition, both olive ridley and leatherback turtles exhibited thermal independence of internesting intervals presumably due to the large body-size of leatherback turtles and the unique capacity of ridley turtles to delay oviposition. The observed interspecific differences in the relationship between the length of the internesting interval and water temperatures indicate the complex and variable responses that each sea turtle species may exhibit due to environmental fluctuations and climate change.
Long dive capacity of olive ridley turtles (Lepidochelys olivacea) at high water temperature during the post-nesting foraging period in the Arafura Sea
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Water temperature and body size are considered to be important factors influencing the diving capabilities of ectothermic reptiles. Although high water temperature and small body size tend to cause short dive durations, previous studies have reported that olive ridley turtles, the smallest sea turtle species distributed in tropical regions, often conduct prolonged dives. To understand diving behavior during the post-nesting foraging periods, especially the relationship between dive duration and water temperature for this species, satellite relay data loggers were attached to 10 nesting females (straight carapace length: 60.5 ± 2.6 cm, estimated body mass: 30.5 ± 4.0 kg) in West Papua, Indonesia, in 2017 and 2019. During the post-nesting tracking period (34–153 days), the turtles migrated southward to the Arafura Sea. A total of 9469 dives were observed, and 28.9% of the dives were longer than 1 h (mean: 44.0 ± 33.1 min, max: 220 min), although the turtles experienced high water temperatures (25.5 ± 2.6 °C). The behavioral aerobic dive limits (behavioral ADLs) calculated from the relationship between the dive depth and duration of olive ridley turtles were 89.6 min and 167.7 min for V-shaped and U-shaped dives, respectively. Even for dives above the behavioral ADL (1.8% for V-shaped and 2.0% for U-shaped dives), the turtles dove 1.1 ± 0.1 (max: 1.6) and 1.1 ± 0.1 (max: 1.3) times longer than the behavioral ADLs for V-shaped and U-shaped dives, respectively. On the other hand, the calculated ADLs (cADLs), estimated from the metabolic rates and oxygen stores of loggerhead turtles, were 51.2 ± 20.3 min (range: 24.1–139.3 min) and 99.8 ± 38.5 min (range: 39.4–258.3 min) for V-shaped and U-shaped dives, respectively. The turtles often exceeded the cADLs (21.4–29.1% for V-shaped dives and 21.2–42.2% for U-shaped dives), and they dove 1.4 ± 0.3 (max: 3.1) and 1.3 ± 0.3 (max: 3.4) times longer than the cADLs for V-shaped and U-shaped dives, respectively. However, those long dives were not considered anaerobic because of the short post-dive surface durations (4.7 ± 5.8 min). Additionally, the relationship between dive duration and water temperature indicated that olive ridley turtles dove longer than loggerhead and green turtles in the high temperature range (> 20 °C). This study confirms that the diving capacity of olive ridley turtles is qualitatively different from those of loggerhead and green turtles for several reasons, such as low metabolic rates and/or low activity levels at high water temperatures.
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What makes marine turtles go: A review of metabolic rates and their consequences

Abstract

Section snippets

Understanding The Fire of Life

Overview of methods to obtain metabolic rates

Comparison of MRs among species and life stages

Applications of MR measurements to marine turtle ecology

Future directions

Acknowledgments

Activity metabolism of the lower vertebrates

Annu. Rev. Physiol.

The energetics of reptilian activity

Physiological adjustements to prolonged diving in the Pacific green turtle (Chelonia mydas agassizii)

Comp. Biochem. Physiol.

The consequences of herbivory for the life history pattern of the Caribbean green turtle, Chelonia mydas

Reports of sea turtles from New England and eastern Canada

Can. Field-Nat.

Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny

Science

Exercise warms adult leatherback turtles

Comp. Physiol. Biochem., Part A

Behavioral inference of diving metabolic rate in free-ranging leatherback turtles

Physiol. Biochem. Zool.

Toward a metabolic theory of ecology

Ecology

Metabolic regulation in diving birds and mammals

Resp. Physiol. Neurobiol.,

Respiratory, cardiovascular and metabolic adjustments during steady state swimming in the green turtle, Chelonia mydas

J. Comp. Physiol., B

Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods

Funct. Ecol.

Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration

J. Exp. Biol.

Energetics during hatchling dispersal of the olive ridley turtle Lepidochelys olivacea using doubly labeled water

Physiol. Biochem. Zool.

Temperature tolerances in the American alligator and their bearing on the habits, evolution, and extinction of the dinosaurs

Bull. Am. Mus. Nat. Hist.

Proximate and evolutionary constraints on energy relations of reptiles

Physiol. Zool.

Energy budgets and life histories of reptiles

Methods for studying the energetics of freely diving animals

Can. J. Zool.

Aerobic dive limit: how often does it occur in nature?

Comp. Biochem. Physiol., Part A

Temperature and the life-history strategies of sea turtles

J. Therm. Biol.

Feeding, gut dynamics, digestion, and O2 consumption in hatchling green turtles (Chelonia mydas)

Br. J. Herpetol.

Individuality of growth, appetite, metabolic rate, and assimilation of nutrients in young green turtles (Chelonia mydas L.)

Herpetol. J.

Oxygen uptake and heart rate in young green turtles (Chelonia mydas)

J. Zool. London

Thermal and biochemical characteristics of the lipids of the leatherback turtle Dermochelys coriacea: evidence of endothermy

J. Mar. Biol. Assoc. U.K.

The energy density of jellyfish: estimates from bomb-calorimetry and proximate-composition

J. Exp. Mar. Biol. Ecol.

Interfaces between biophysical and physiological ecology and the population ecology of terrestrial verterbrate ectotherms

Physiol. Zool.

Swim speed and movement patterns of gravid leatherback sea turtles (Dermochelys coriacea) at St. Croix, US Virgin Islands

J. Exp. Biol.

Distribution of juvenile leatherback sea turtle Dermochelys coriacea sightings

Mar. Ecol. Prog. Ser.

One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems

J. Appl. Physiol.

Body temperature of Dermochelys coriacea: warm turtle from cold water

Science

Respirometry, the gold standard

The Physiologist

Atlantic leatherback turtles, Dermochelys coriacea, in cold water off Newfoundland and Labrador

Can. Field-Nat.

Brown adipose tissue in leatherback sea turtles: a thermogenic organ in an endothermic reptile

Copeia

Anatomical evidence for a countercurrent heat exchanger in the leatherback turtle (Dermochelys coriacea)

Nature

Time constants of heating and cooling in the eastern water dragon, Physignathus lesueruii, and some generalizations about heating and cooling in reptiles

J. Therm. Biol.

Only some like it hot — quantifying the thermal niche of the loggerhead sea turtle

Divers. Distrib

The implications of variable remigration intervals for the assessment of population size in sea turtles

J. Theor. Biol.

Feeding, gut dynamics, digestion, and O₂ consumption in hatchling green turtles (Chelonia mydas)

One-step N₂-dilution technique for calibrating open-circuit VO₂ measuring systems

Long-term cold acclimation leads to high Q₁₀ effects on oxygen consumption of loggerhead sea turtles Caretta caretta