Dietary protein requirement for captive juvenile green turtles (Chelonia mydas)

Head-starting programs are extremely important for restoring the population of sea turtles in wild whereas husbandry conditions and feeding regimens of captive turtles are still limited. In the current study, the optimal dietary protein requirement for green turtle (Chelonia mydas) was investigated to support rearing in head-starting programs. Twenty-five-day-old turtles (44.5–46.2 g body weight, n = 45) were randomly distributed into 15 experimental plastic tanks, comprising three treatment replications of 3 turtles each. They were fed fishmeal-based feeds containing different levels of protein (30%, 35%, 40%, 45%, and 50%) for 8 weeks. At the end of feeding trial, growth performance (specific growth rate = 1.86% body weight/day) and feed utilization (protein efficiency ratio = 3.30 g gain/g protein) were highest in turtles fed with 40% protein in feed (p < .05). These nutritional responses were significantly supported by specific activities of fecal digestive enzymes, especially trypsin, chymotrypsin, amylase, and the amylase/trypsin ratio. Also, this dietary level improved the deposition of calcium and phosphorus in carapace, supporting a hard carapace and strong healthy bones. There were no negative effects in general health status of reared turtles, as indicated by hematological parameters. Based on a broken-line analysis between dietary protein levels and specific growth rate, the optimal protein level for green turtles was estimated as 40.6%. Findings from the current study support the use of artificial diets of specific protein levels to rear captive green turtle before release to natural habitats.     

Evolution of bite performance in turtles

Abstract Among vertebrates, there is often a tight correlation between variation in cranial morphology and diet. Yet, the relationships between morphological characteristics and feeding performance are usually only inferred from biomechanical models. Here, we empirically test whether differences in body dimensions are correlated with bite performance and trophic ecology for a large number of turtle species. A comparative phylogenetic analysis indicates that turtles with carnivorous and durophagous diets are capable of biting harder than species with other diets. This pattern is consistent with the hypothesis that an evolutionary increase in bite performance has allowed certain turtles to consume harder or larger prey. Changes in carapace length tend to be associated with proportional changes in linear head dimensions (no shape change). However, maximum bite force tends to change in proportion to length cubed, rather than length squared, implying that changes in body size are associated with changes in the design of the jaw apparatus. After the effect of body size is accounted for in the analysis, only changes in head height are significantly correlated with changes in bite force. Additionally, our data suggest that the ability to bite hard might trade off with the ability to feed on fast agile prey. Rather than being the direct result of conflicting biomechanical or physiological demands for force and speed, this trade‐off may be mediated through the constraints imposed by the need to retract the head into the shell for defensive purposes.     

Driftnet fishery threats sea turtles in the Atlantic Ocean

Fisheries are recognised as a major threat to sea turtles worldwide. Oceanic driftnets are considered the main cause of the steep decline in Pacific Ocean populations of the leatherback sea turtle Dermochelys coriacea. The world’s largest leatherback population nests in West Africa and migrates across the Atlantic Ocean to feed off the South American coast. There, the turtles encounter a range of fisheries, including the Brazilian driftnet fishery targeting hammerhead sharks. From 2002 to 2008, 351 sea turtles were incidentally caught in 41 fishing trips and 371 sets. Leatherbacks accounted for 77.3% of the take (n = 252 turtles, capture rate = 0.1405 turtles/km of net), followed by loggerheads Caretta caretta (47 individuals, capture rate = 0.0262 turtles/km of net), green turtles Chelonia mydas (27 individuals, capture rate = 0.0151 turtles/km of net) and unidentified hard-shelled turtles (25 individual, capture rate = 0.0139 turtles/km of net) that fell off the net during hauling. Immediate mortality (i.e., turtles that were dead upon reaching the vessel, excluding post-release mortality) was similar among the species and accounted for 22.2 to 29.4% of turtles hauled onboard. The annual catch by this fishery ranged from 1,212 to 6,160 leatherback turtles, as estimated based on bootstrap procedures under different fishing effort scenarios in the 1990s. The present inertia in law and enforcement regarding gillnet regulations in Brazil could result in the reestablishment of the driftnet fishery, driving rates of leatherback mortality to levels similar to those observed in previous decades. This development could potentially lead to the collapse of the South Atlantic leatherback population, mirroring the decline of the species in the Pacific. In light of these potential impacts and similar threats to other pelagic mega fauna, we recommend banning this type of fishery in the region.     

Metabolic scaling in turtles

Bennett and Dawson (1976) presented an analysis of the relationship of metabolic rate (MR) and body mass among turtles, based on 10 studies, but unlike most of other groups of ectotherms, there has been no update to include the many later reports on turtles. Here I present a review of the data on turtle metabolic rates at 20, 25, and 30 °C, along with regression equations and graphical analyses from a large number of studies. Two generalities emerge: (1) reported metabolic rates for sea turtles are higher than for other chelonians, although it is not certain whether this is an intrinsic characteristic of sea turtles or an artifact related to experimental conditions (such as greater activity of sea turtles in metabolic chambers and the fact that a number of studies were done with the turtles out of water), and (2) the slopes of the log–log plots of metabolic rate (MR) vs. body mass [b in the allometric equation MR = a(mass)^b] are mostly lower than previously reported in smaller studies.     

Venous blood gases and lactates of wild loggerhead sea turtles (Caretta caretta) following two capture techniques

During summer of 2001, venous blood gases were determined in loggerhead sea turtles (Caretta caretta) captured by trawl (n = 16) in coastal waters of South Carolina and Georgia (USA) as part of a sea turtle census program and captured in pound nets (n = 6) in coastal North Carolina (USA) during a study of sea turtle population biology. Trawls were towed for 30 min, so turtles captured were forcibly submerged for < or = 30 min. Pound nets are passive gear in which fish and sea turtles are funneled into a concentrated area and removed periodically. Sea turtles in pound nets are free to surface and to feed at will. Blood was obtained from the dorsal cervical sinus as quickly as possible after landing on the boat (range 2-10 min trawl, 1-2 min pound net) and at 30 min after landing just prior to release. Blood gases including pH, partial pressures of O2 and CO2 (pO2, pCO2), and lactate were measured within 10 min. Instrument measurements for pH, pO2, and pCO2 made at 37 C were corrected to cloacal temperature and HCO3- was calculated from temperature-corrected pH and pCO2. Venous blood pH and bicarbonate were higher, and pO2 and lactate were lower from pound net-captured turtles compared to trawl captured turtles at the initial sampling time. In pound net turtles, pH and bicarbonate declined and lactate increased during 30 min on deck. In trawled sea turtles, venous blood pH increased and pCO2 and pO2 decreased during the 30 min on deck. Both capture systems caused perturbations in blood gas, acid-base, and lactate status, though alterations were greater in trawl captured turtles.     

The ecology of overwintering among turtles: where turtles overwinter and its consequences

Turtles are a small taxon that has nevertheless attracted much attention from biologists for centuries. However, a major portion of their life cycle has received relatively little attention until recently - namely what turtles are doing, and how they are doing it, during the winter. In the northern parts of their ranges in North America, turtles may spend more than half of their lives in an overwintering state. In this review, I emphasise the ecological aspects of overwintering among turtles, and consider how overwintering stresses affect the physiology, behaviour, distributions, and life histories of various species.Sea turtles are the only group of turtles that migrate extensively, and can therefore avoid northern winters. Nevertheless, each year a number of turtles, largely juveniles, are killed when trapped by cold fronts before they move to safer waters. Evidently this risk is an acceptable trade-off for the benefits to a population of inhabiting northern developmental habitats during the summer.Terrestrial turtles pass the winter underground, either in burrows that they excavate or that are preformed. These refugia must provide protection against desiccation and lethal freezing levels. Some burrows are extensive (tortoise genus Gopherus), while others are shallow, or the turtles may simply dig into the ground to a safe depth (turtle genus Terrapene). In the latter genus, freeze tolerance may play an adaptive role.Most non-marine aquatic turtles overwinter underwater, although Clemmys (Actinemys) marmorata routinely overwinters on land when it occurs in riverine habitats, Kinosternon subrubrum often overwinters on land, and several others may overwinter terrestrially on occasion, especially in more southern climates. For northern species that overwinter underwater, there are two physiological groupings, those that are anoxia-tolerant and those that are relatively anoxia-intolerant. All species fare well physiologically in water with a high partial pressure of oxygen (PO2). A lack of anoxia tolerance limits the types of habitats that a freshwater turtle may live in, since unlike sea turtles, they cannot travel long distances to hibernate.Hatchlings of some species of turtles spend their first winter in or below the nest cavity, while hatchlings of other species in the same area, including northern areas, emerge in the autumn and presumably hibernate underwater. All hatchlings are relatively anoxia-intolerant, and there are no studies to date of where hatchling turtles that do not overwinter in or below the nest cavity spend their first winter. Equally little is known of the ontogeny of anoxia tolerance, other than that adults of all species are more anoxia-tolerant than their hatchlings, probably because of their better ossified shells, which provide adults with more buffer reserves and a larger site in which to sequester lactate. The northern limits of turtles are most likely determined by reproductive limitations (time for egg-laying, incubation, and hatching) than by the rigors of hibernation.Mortality is typically lower in turtle populations during hibernation than it is during their active periods. However, episodic mortality events do occur during hibernation, due to freezing, prolonged anoxia, or predation.     

The role of turtles as coral reef macroherbivores

Herbivory is widely accepted as a vital function on coral reefs. To date, the majority of studies examining herbivory in coral reef environments have focused on the roles of fishes and/or urchins, with relatively few studies considering the potential role of macroherbivores in reef processes. Here, we introduce evidence that highlights the potential role of marine turtles as herbivores on coral reefs. While conducting experimental habitat manipulations to assess the roles of herbivorous reef fishes we observed green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) showing responses that were remarkably similar to those of herbivorous fishes. Reducing the sediment load of the epilithic algal matrix on a coral reef resulted in a forty-fold increase in grazing by green turtles. Hawksbill turtles were also observed to browse transplanted thalli of the macroalga Sargassum swartzii in a coral reef environment. These responses not only show strong parallels to herbivorous reef fishes, but also highlight that marine turtles actively, and intentionally, remove algae from coral reefs. When considering the size and potential historical abundance of marine turtles we suggest that these potentially valuable herbivores may have been lost from many coral reefs before their true importance was understood.     

Gulps, wheezes, and sniffs: how measurement of beak movement in sea turtles can elucidate their behaviour and ecology

This study was performed to assess the extent to which an intermandibular angle sensor (IMASEN) may be used to elucidate the behaviour of six captive loggerhead turtles. The measuring system was glued to the beak of turtles and set to measure the intermandibular distance at 5 Hz while the turtles fed (on anchovies, squid, and live crabs), swam, rested, and breathed. The behaviour of the equipped turtles was filmed and compared afterwards to the sensor readings. The IMASEN output data allowed quantification of the number of food items ingested as well as the time between food seizure and deglutition and the type of food ingested. However, nonfeeding turtles exhibited regular jaw movements with a reduced amplitude of ca. 2.2 mm, which clearly differed from feeding movements and were caused by buccal oscillations. Such movements of the base of the buccal cavity generate a steady flow of water pass the chemosensory organs and were interrupted only during food ingestion, resting, and breathing. Breathing was clearly distinguishable by the IMASEN. The beak sensor is thus a reliable system to investigate a number of behaviours in sea turtles which encompass foraging, buccal oscillation, and respiratory frequency. It has potential for allocating time to different activities in free-ranging sea turtles and thus allows us to gain insight to their foraging and diving strategies.     

Island-finding ability of marine turtles

Green turtles (Chelonia mydas) swim from foraging grounds along the Brazilian coast to Ascension Island to nest, over 2200 km distant in the middle of the equatorial Atlantic. To test the hypothesis that turtles use wind-borne cues to locate Ascension Island we found turtles that had just completed nesting and then moved three individuals 50 km northwest (downwind) of the island and three individuals 50 km southeast (upwind). Their subsequent movements were tracked by satellite. Turtles released downwind returned to Ascension Island within 1, 2 and 4 days, respectively. By contrast, those released upwind had far more difficulty in relocating Ascension Island, two eventually returning after 10 and 27 days and the third heading back to Brazil after failing to find its way back to the island. These findings strongly support the hypothesis that wind-borne cues are used by turtles to locate Ascension Island.     

Respiration in neonate sea turtles

The pattern and control of respiration is virtually unknown in hatchling sea turtles. Using incubator-raised turtles, we measured oxygen consumption, frequency, tidal volume, and minute volume for leatherback (Dermochelys coriacea) and olive ridley (Lepidochelys olivacea) turtle hatchlings for the first six days after pipping. In addition, we tested the hatchlings' response to hypercapnic, hyperoxic, and hypoxic challenges over this time period. Hatchling sea turtles generally showed resting ventilation characteristics that are similar to those of adults: a single breath followed by a long respiratory pause, slow frequency, and high metabolic rate. With hypercapnic challenge, both species responded primarily by elevating respiratory frequency via a decrease in the non-ventilatory period. Leatherback resting tidal volume increased with age but otherwise, neither species' resting respiratory pattern nor response to gas challenge changed significantly over the first few days after hatching. At the time of nest emergence, sea turtles have achieved a respiratory pattern that is similar to that of actively diving adults.     

Natural beaches confer fitness benefits to nesting marine turtles

Coastal ecosystems provide vital linkages between aquatic and terrestrial habitats and thus support extremely high levels of biodiversity. However, coastlines also contain the highest densities of human development anywhere on the planet and are favoured destinations for tourists, creating a situation where the potential for negative effects on coastal species is extremely high. I gathered data on marine turtle reproductive output from the literature to determine whether coastal development negatively influences offspring production. Female loggerhead (Caretta caretta) and green turtles (Chelonia mydas) nesting on natural beaches (as opposed to beaches with permanent development) produce significantly more hatchling turtles per nest; all else being equal, females that successfully produce more offspring will have higher fitness than conspecifics producing fewer offspring. Thus, female marine turtles nesting on natural beaches probably have higher fitness than turtles nesting on developed beaches. Consequently, populations nesting on natural beaches may be able to recover more quickly from the historic population declines that have plagued marine turtles, and some species may recover more quickly than others.     

Pareiasaur phylogeny and the origin of turtles

The evolutionary relationship of all the valid species (and thus genera) of pareiasaurs are assessed through a phylogcnctic analysis of these taxa together with turtles, Owenetta, Barasaurus, Sclerosaurus, procolophonids, lanthanosuchids, nyctiphruretids, and nycterolctcrids. 128 os-teological characters were used, and almost all relevant taxa were examined. The results confirm that among these taxa, pareiasaurs and turtles form a robust clade, to the exclusion of all other taxa including procolophonids. However, pareiasaurs might not be the mono-phyletic sister group of turtles, as previously suggested. Rather, there is some evidence that pareiasaurs are paraphyletic with respect to (i.e. ‘ancestral to’) turtles. Among pareiasaurs, the early, large, heavily ossified forms such as Brady.saurus are most distantly related to turtles. These forms are characterized by rather smooth skulls, and dermal armour restricted to the dorsal midline. More closely related to turtles are forms such as Scutosaurus, Pareiasuchus, and Elginia. These taxa form a distinct clade of pareiasaurs, characterized by a very ‘mammallike’ pelvis, elaborate cranial ornamentation and a loose covering of osteoderms over the entire dorsum. The late, dwarf pareiasaurs Nanoparia, Anthodon, and Pumiliopareia are the nearest relatives of turtles. These forms exhibit otherwise uniquely turtle features such as a rigid covering of dermal armour over the entire dorsal region, expanded flattened ribs, cylindrical scapula blade, great reduction of humeral torsion (to 25^o), greatly developed trochanter major, offset femoral head, and reduced cnemial crest of the tibia. Thus, many features thought to be restricted to turtles (and thus to have evolved simultaneously with the turtle shell) actually arose earlier, at various points along the pareiasaurian stem lineage. The identification of the nature and sequence of anatomical changes leading to the origin of turtles, and the possibility that turtles are derived from dwarf pareiasaurs, should have important implications for speculations on the evolutionary biology of turtle origins.     

Hemoprotozoa of freshwater turtles in Queensland

Blood smears from 27 turtles (15 Emydura signata, nine Elseya latisternum, and three Chelodina longicollis) from southeastern Queensland (Australia) were examined for infections by hemoprotozoan parasites between January and June 1999. Infections were found in 26 (96%) of the turtles. Twenty five (93%) were infected with the adeleorin coccidian Haemogregarina clelandi, eight (30%) with the hemosporidian Haemoproteus chelodinae, 11 (41%) with the kinetoplastid flagellate Trypanosoma chelodinae, and eight (30%) with a novel Trypanosoma sp. Despite the high prevalence and intensity of infections, there was no evidence of clinical disease in any of the turtles.     

Variation in reproductive output of marine turtles

Most marine turtle species are non-annual breeders and show variation in both the number of eggs laid per clutch and the number of clutches laid in a season. Large levels of inter-annual variation in the number of nesting females have been well documented in green turtle nesting populations and may be linked to environmental conditions. Other species of marine turtle exhibit less variation in nesting numbers. This inter-specific difference is thought to be linked to trophic status. To examine whether individual reproductive output is more variable in the herbivorous green turtle (Chelonia mydas Linneaeus 1758) than the carnivorous loggerhead (Caretta caretta Linneaeus 1758), we examined the nesting of both species in Cyprus over nine seasons. Green turtles showed slower annual growth rates (0.11 cm year⁻¹ curved carapace length (CCL) and 0.27 cm year⁻¹ curved carapace width (CCW)) than loggerhead turtles (0.36 cm year⁻¹ CCL, 0.51 cm year⁻¹ CCW). CCL was highly correlated to mean clutch size in both green (R²=0.51) and loggerhead turtles (R²=0.61) and maximal clutch size of green turtles (R²=0.58). Larger females did not lay a greater number of clutches or have a shorter remigration interval than smaller females of either species. On average, the size of green turtle clutches increased and that of loggerhead turtles decreased as the season progressed. Individual green turtles, however, produced more eggs per clutch through the season to a maximum in the third or fourth clutch. In loggerhead turtles, clutches 1-4 were very similar in size but the fifth clutch was 38% smaller than the first. No individuals of either species were recorded laying more than five clutches. Green turtles may not be able to achieve their maximum reproductive output with respect to clutch size throughout the season, whereas only loggerhead turtles laying five clutches (n=5) appear to become resource depleted. Green turtles nesting in years when large numbers of nests were recorded laid a greater number of clutches than females nesting in years with lower levels of nesting.     

Characterizing watercraft-related mortality of sea turtles in Florida

Mortality from being struck by a motorized watercraft is considerable for many aquatic vertebrates around the world, including sea turtles. We studied stranded (i.e., dead, sick, or injured) sea turtles found in Florida, USA, during 1986–2014 and identified those with sharp force or blunt force injuries indicative of a vessel strike. About a third of stranded loggerheads (Caretta caretta), green turtles (Chelonia mydas), and leatherbacks (Dermochelys coriacea) had a vessel-strike injury (VSI). The frequency of this injury was lower but still substantial for stranded Kemp's ridleys (Lepidochelys kempii; 26.1%) and hawksbills (Eretmochelys imbricata; 14.8%). Over the study period, the annual number of stranded loggerheads, green turtles, and Kemp's ridleys with a VSI increased as did the annual number of vessels registered in Florida. Eighty-one percent of the stranded turtles with a VSI were found in the southern half of Florida and 66% of those were found along the southeast coast. By coastal county, the proportion of stranded sea turtles with a VSI was positively related to the mean annual number of registered vessels. The percentage occurrence of a VSI was highest for adult loggerheads, green turtles, and leatherbacks, and reproductively active individuals appeared to be particularly vulnerable to these injuries. We conducted necropsies on 194 stranded sea turtles with a VSI and concluded that this injury was the cause of death or the probable cause of death in ≥92.8% of these cases. During 2000–2014, we estimate that the mean annual numbers of stranded sea turtles that died from a VSI were 142–229 loggerheads, 101–162 green turtles, 16–32 Kemp's ridleys, 4–6 leatherbacks, and 2–4 hawksbills. Considering that only about 10–20% of sea turtles that died likely washed ashore, the overall annual mortality may have been 5–10 times greater than that represented by strandings. Most of the significant clusters of stranded sea turtles with a VSI occurred at inlets or passes and the probability that a stranded sea turtle had a VSI decreased with increasing distance from inlets or passes, navigable waterways, and marinas. We suggest focusing initial management efforts on reducing watercraft-related mortality for all sea turtle species around 8 inlets in southeast Florida, reproductively active loggerheads and green turtles along the coast of southeast Florida, and Kemp's ridleys and adult male loggerheads at passes along the coast of southwest Florida. Published 2019. This article is a U.S. Government work and is in the public domain in the USA. The Journal of Wildlife Management published by Wiley Periodicals, Inc. on behalf of The Wildlife Society     

Transitional fossils and the origin of turtles

The origin of turtles is one of the most contentious issues in systematics with three currently viable hypotheses: turtles as the extant sister to (i) the crocodile–bird clade, (ii) the lizard–tuatara clade, or (iii) Diapsida (a clade composed of (i) and (ii)). We reanalysed a recent dataset that allied turtles with the lizard–tuatara clade and found that the inclusion of the stem turtle Proganochelys quenstedti and the ‘parareptile’ Eunotosaurus africanus results in a single overriding morphological signal, with turtles outside Diapsida. This result reflects the importance of transitional fossils when long branches separate crown clades, and highlights unexplored issues such as the role of topological congruence when using fossils to calibrate molecular clocks.     

Arsenic accumulation in three species of sea turtles

Arsenic in the liver, kidney and muscle of three species of sea turtles, e.g., green turtles (Chelonia mydas), loggerhead turtles (Caretta caretta) and hawksbill turtles (Eretmochelys imbricata), were determined using HG-AAS, followed by arsenic speciation analysis using HPLC-ICP-MS. The order of arsenic concentration in tissues was muscle > kidney > liver. Unexpectedly, the arsenic concentrations in the hawksbill turtles feeding mainly on sponges were higher than the two other turtles primarily eating algae and mollusk which accumulate a large amount of arsenic. Especially, the muscles of the hawksbill turtles contained remarkably high arsenic concentrations averaging 153 mg kg^–1 dry weight with the range of 23.1–205 mg kg^–1 (n=4), even in comparison with the data from other organisms. The arsenic concentrations in the tissues of the green turtles were significantly decreased with standard carapace length as an indicator of growth. In arsenic compounds, arsenobetaine was mostly detected in the tissues of all the turtles. Besides arsenobetaine, a small amount of dimethylarsinic acid was also observed in the hawksbill turtles.     

Modifications of traps to reduce bycatch of freshwater turtles

Mortality of freshwater turtles varies among types and deployments of traps. There are few or no losses in hoop or fyke traps set where turtles may reach air, including placement in shallows, addition of floats on traps, and tying traps securely to a stake or to shore. Turtle mortality occurs when traps are set deep, traps are checked at intervals >1 day, and when turtles are captured as bycatch. Devices are available that exclude turtles from traps set for crab or game fish harvest. Slotted gates in front of the trap mouth reduce turtle entry, but small individuals still may be trapped. Incidental take of turtles is preventable by integrating several designs into aquatic traps, such as adding floats to the top of traps so turtles may reach air or an extension tube (chimney, ramp) that creates an escape route. © 2010 The Wildlife Society.     

Vertical niche overlap by two ocean giants with similar diets: Ocean sunfish and leatherback turtles

We used satellite tags to record the patterns of depth utilisation for four ocean sunfish (Mola mola) and two leatherback turtles (Dermochelys coriacea) moving in broadly the same area off South Africa. Individuals were tracked for between 2 and 8 months and dive data relayed via satellite. For all the sunfish and one of the turtles, we received binned data on depth distribution, while for the second turtle we received individual dive profiles along with the proportion of time spent diving. Leatherback turtles dived almost exclusively within the upper 200 m, spending only 0.6 and 0.2% of their time > 200 m. There were times when sunfish likewise occupied these relatively shallow depths. However, there were also protracted periods when sunfish spent the majority of their time much deeper, with one individual remaining around 500 m for many hours at a time. These results suggest that sunfish sometimes exploit deeply distributed prey which is beyond the foraging range of leatherback turtles. We conclude that while both species are believed to feed predominantly on gelatinous zooplankton, the fact that sunfish do not need to come to the surface to breathe means that they can occupy an expanded vertical niche compared to the leatherback turtle.