Response of heart rate and cloacal ventilation in the bimodally respiring freshwater turtle, Rheodytes leukops, to experimental changes in aquatic PO2

Changes in heart rate (f _H) and cloacal ventilation frequency (f _C) were investigated in the Fitzroy turtle, Rheodytes leukops, under normoxic (17.85 kPa) and hypoxic (3.79 kPa) conditions at 25°C. Given R. leukops’ high reliance on aquatic respiration via the cloacal bursae, the objective of this study was to examine the effect of varying aquatic PO₂ levels upon the expression of a bradycardia in a freely diving, bimodally respiring turtle. In normoxia, mean diving f _H and f _C for R. leukops remained constant with increasing submergence length, indicating that a bradycardia failed to develop during extended dives of up to 3 days. Alternatively, exposure to aquatic hypoxia resulted in the expression of a bradycardia as recorded by a decreasing mean diving f _H with increasing dive duration. The observed bradycardia is attributed to a hypoxic-induced metabolic depression, possibly facilitated by a concurrent decrease in f _C. Results suggest that R. leukops alters its strategy from aquatic O₂ extraction via cloacal respiration in normoxia to O₂ conservation when exposed to aquatic hypoxia for the purpose of extending dive duration. Upon surfacing, a significant tachycardia was observed for R. leukops regardless of aquatic PO₂, presumably functioning to rapidly equilibrate blood and tissue gas tensions with alveolar gas to reduce surfacing duration.     

The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula

In aquatic vertebrates that acquire oxygen aerially dive duration scales positively with body mass, i.e. larger animals can dive for longer periods, however in bimodally respiring animals the relationship between dive duration and body mass is unclear. In this study we investigated the relationships between body size, aquatic respiration, and dive duration in the bimodally respiring turtle, Elseya albagula. Under normoxic conditions, dive duration was found to be independent of body mass. The dive durations of smaller turtles were equivalent to that of larger individuals despite their relatively smaller oxygen stores and higher mass specific metabolic rates. Smaller turtles were able to increase their dive duration through the use of aquatic respiration. Smaller turtles had a relatively higher cloacal bursae surface area than larger turtles, which allowed them to extract a relatively larger amount of oxygen from the water. By removing the ability to respire aquatically (hypoxic conditions), the dive duration of the smaller turtles significantly decreased restoring the normal positive relationship between body size and dive duration that is seen in other air-breathing vertebrates.     

Blood-respiratory and acid–base changes during extended diving in the bimodally respiring freshwater turtle<Emphasis Type="Italic"> Rheodytes leukops</Emphasis>

Changes in blood-gas, acid–base, and plasma-ion status were investigated in the bimodally respiring turtle, Rheodytes leukops, during prolonged dives of up to 12 h. Given that R. leukops routinely submerges for several hours, the objective of this study was to determine whether voluntarily diving turtles remain aerobic and simultaneously avoid hypercapnic conditions over increasing dive lengths. Blood PO₂, PCO₂, and pH, as well as plasma concentrations of lactate, glucose, Na⁺, K⁺, Cl^–, total Ca, and total Mg were determined in venous blood collected from the occipital sinus. Blood PO₂ declined significantly with dive length; however, oxy-haemoglobin saturation remained greater than 30% for all R. leukops sampled. No changes were observed in blood PCO₂, pH, [HCO₃^–], or plasma glucose, with increasing dive length. Despite repeated dives lasting more than 2 h, plasma lactate remained less than 3 mmol l^–1 for all R. leukops sampled, indicating the absence of anaerobiosis. Compensatory acid–base adjustments associated with anaerobiosis (e.g. declining [Cl^–], increasing total [Ca] and [Mg]) were likewise absent, with plasma-ion concentrations remaining stable with increasing dive length. Results indicate that R. leukops utilises aquatic respiration to remain aerobic during prolonged dives, thus effectively avoiding the development of a metabolic and respiratory acidosis.     

Thermal plasticity of diving behavior, aquatic respiration, and locomotor performance in the Mary River turtle Elusor macrurus

Locomotion is a common measure of performance used in studies of thermal acclimation because of its correlation with predator escape and prey capture. However, for sedentary animals such as freshwater turtles, we propose that diving behavior may be a more ecologically relevant measure of performance. Increasing dive duration in hatchling turtles reduces predator exposure and therefore functions as an ecological benefit. Diving behavior is thermally dependent, and in some species of freshwater turtles, it is also reliant on aquatic respiration. This study examined the influence of thermal acclimation on diving behavior, aquatic respiration, and locomotor performance in the endangered, bimodally respiring Mary River turtle Elusor macrurus. Diving behavior was found to partially acclimate at 17 degrees C, with turtles acclimated to a cold temperature (17 degrees C) having a significantly longer dive duration than hatchlings acclimated to a warm temperature (28 degrees C). This increase in dive duration at 17 degrees C was not a result of physiological alterations in metabolic rate but was due instead to an increase in aquatic oxygen consumption. Increasing aquatic oxygen consumption permitted cold-acclimated hatchlings to remain submerged for significantly longer periods, with one turtle undertaking a dive of over 2.5 d. When burst-swimming speed was used as the measure of performance, thermal acclimation was not detected. Overall, E. macrurus demonstrated a partial ability to acclimate to changes in environmental temperature.     

Diving behaviour, aquatic respiration and blood respiratory properties: a comparison of hatchling and juvenile Australian turtles

Australia has a number of bimodally respiring freshwater turtle species that use aquatic respiration to extend their aerobic dive limit. While species variations in reliance on aquatic respiration are reflected in the diving behaviour and ecology of adults, it is unknown whether these relationships also occur in hatchling and juvenile turtles. This study compared the diving behaviour, aquatic respiration and blood respiratory properties of hatchling and juveniles from five species of Australian freshwater turtles: Rheodytes leukops , Elusor macrurus , Elseya albagula , Elseya latisternum and Emydura signata . Both diving behaviour and physiology differed significantly between species as well as age classes. Dive duration in R. leukops was 17 times longer than the other species, with two hatchlings remaining submerged for the entire 72 h recording period. The long dive duration recorded for R. leukops was supported by a high reliance on aquatic respiration (63–73%) and high blood oxygen affinity ( P ₅₀=17.24 mmHg). A correlation between dive duration, aquatic respiration and blood respiratory properties was not observed in the remaining turtle species where, despite the longer dive duration of Els. albagula and Elu. macrurus compared with Em. signata and Els. latisternum , there was no difference observed in per cent aquatic respiration or blood oxygen affinity between these species. When compared with adult individuals (data from previous studies), dive duration was positively correlated with body size in Em. signata , Els. albagula and R. leukops , but a negative relationship occurred in Els. latisternum and Elu. macrurus .     

Implications of river damming: the influence of aquatic hypoxia on the diving physiology and behaviour of the endangered Mary River turtle

River impoundments are characterized by low oxygen levels as a result of reduced water velocity and increased water depth. Bimodally respiring turtle species are likely to be highly sensitive to changes in aquatic PO₂ with decreases in oxygen levels impacting upon their diving ability. The acute and long-term effects of aquatic hypoxia on dive duration, oxygen consumption and blood respiratory properties were examined in hatchlings of the endangered Mary River turtle Elusor macrurus . It was hypothesized that acute exposure to aquatic hypoxia would cause a decrease in dive duration as a consequence of a decrease in reliance on aquatic respiration. With long-term exposure to hypoxia, we predicted that Elu. macrurus would have the capacity to compensate for the acute effect of hypoxia and that dive duration would increase due to an increase in aquatic respiration, haemoglobin concentration and oxygen affinity (P₅₀). When exposed to hypoxic conditions, aquatic respiration in Elu. macrurus was substantially reduced resulting in a 51% decrease in dive duration. Contrary to our predictions, Elu. macrurus hatchlings did not acclimate, and long-term exposure to hypoxic conditions caused Elu. macrurus to lose significantly more oxygen to the hypoxic water than the normoxic acclimated turtles. The exacerbation of long-term hypoxia on the respiratory physiology and diving ecology of Elu. macrurus raises concerns about the impacts of long-term environmental change as a result of habitat alteration on the survival of freshwater turtle populations.     

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.     

Long-term monitoring of leatherback turtle diving behaviour during oceanic movements

The diving behaviour of four leatherback turtles (Dermochelys coriacea) was recorded for periods of 0.5-8.1 months during their postnesting movements in the Indian and Atlantic Oceans, when they covered 1569-18,994 km. Dive data were obtained using satellite-linked transmitters which also provided information on the dive depths and profiles of the turtles. Turtles mainly dove to depths < 200 m, with maximum dive durations under 30-40 min and exhibited diel variations in their diving activity for most part of the routes, with dives being usually longer at night. Diurnal dives were in general quite short, but cases of very deep (> 900 m) and prolonged (> 70 min) dives were however recorded only during daytime. The three turtles that were tracked for the longest time showed a marked change in behaviour during the tracking, decreasing their dive durations and ceasing to dive deeply. Moreover, diel variations disappeared, with nocturnal dives becoming short and numerous. This change in turtle diving activity appeared to be related to water temperature, suggesting an influence of seasonal prey availability on their diving behaviour. The turtle diving activity was independent on the shape of their routes, with no changes between linear movements in the core of main currents or looping segments in presence of oceanic eddies.     

Benefits of thermal acclimation in a tropical aquatic ectotherm,the Arafura filesnake, <Emphasis Type="Italic">Acrochordus arafurae</Emphasis>

The presumption that organisms benefit from thermal acclimation has been widely debated in the literature. The ability to thermally acclimate to offset temperature effects on physiological function is prevalent in ectotherms that are unable to thermoregulate year-round to maintain performance. In this study we examined the physiological and behavioural consequences of long-term exposure to different water temperatures in the aquatic snake Acrochordus arafurae. We hypothesised that long dives would benefit this species by reducing the likelihood of avian predation. To achieve longer dives at high temperatures, we predicted that thermal acclimation of A. arafurae would reduce metabolic rate and increase use of aquatic respiration. Acrochordus arafurae were held at 24 or 32°C for 3 months before dive duration and physiological factors were assessed (at both 24 and 32°C). Although filesnakes demonstrated thermal acclimation of metabolic rate, use of aquatic respiration was thermally independent and did not acclimate. Mean dive duration did not differ between the acclimation groups at either temperature; however, warm-acclimated animals increased maximum and modal dive duration, demonstrating a longer dive duration capacity. Our study established that A. arafurae is capable of thermal acclimation and this confers a benefit to the diving abilities of this snake.     

Juvenile proportion as a predictor of freshwater turtle population change

The extreme longevity of turtles and tortoises can make it difficult to determine the conservation status of their populations because high annual adult survival may mask gradual attrition due to low levels of recruitment. When long-term demographic trends are unknown and available data are insufficient for population modelling, it may be assumed that a scarcity of juveniles indicates low recruitment that will result in population ageing and numerical decline. However, the reliability with which the proportion of juveniles foreshadows demographic change is uncertain. We tested the hypothesis that a low proportion of juveniles in a turtle population presages its ageing by analysing over 20 years of survey data for five discrete populations of the Australian western saw-shelled turtle (Myuchelys bellii: Chelidae), a listed threatened species. The analysis tested whether the initial proportion of juvenile turtles in each population was related to its temporal trend in average body size. The five populations had varied structure and trends, with the initial proportion of juvenile turtles ranging from 10% to 39% and average body size increasing over time in some populations and decreasing in others. Contrary to expectation, the initial proportion of juveniles was unrelated to the trend in average body size and, by inference, average age, indicating that effective trend forecasting requires more detailed demographic information than merely population structure.     

Diving through the thermal window: implications for a warming world

Population decline and a shift in the geographical distribution of some ectothermic animals have been attributed to climatic warming. Here, we show that rises in water temperature of a few degrees, while within the thermal window for locomotor performance, may be detrimental to diving behaviour in air-breathing ectotherms (turtles, crocodilians, marine iguanas, amphibians, snakes and lizards). Submergence times and internal and external body temperature were remotely recorded from freshwater crocodiles (Crocodylus johnstoni) while they free-ranged throughout their natural habitat in summer and winter. During summer, the crocodiles'' mean body temperature was 5.2 ± 0.1°C higher than in winter and the largest proportion of total dive time was composed of dive durations approximately 15 min less than in winter. Diving beyond 40 min during summer required the crocodiles to exponentially increase the time they spent on the surface after the dive, presumably to clear anaerobic debt. The relationship was not as significant in winter, even though a greater proportion of dives were of a longer duration, suggesting that diving lactate threshold (DLT) was reduced in summer compared with winter. Additional evidence for a reduced DLT in summer was derived from the stronger influence body mass exerted upon dive duration, compared to winter. The results demonstrate that the higher summer body temperature increased oxygen demand during the dive, implying that thermal acclimatization of the diving metabolic rate was inadequate. If the study findings are common among air-breathing diving ectotherms, then long-term warming of the aquatic environment may be detrimental to behavioural function and survivorship.     

Impacts of river alteration for flood control on freshwater turtle populations

The impacts of artificial river alteration for flood control on the dynamics of freshwater turtle populations were studied in small urban and rural river systems in northwestern Chiba Prefecture, Japan, from 2003 to 2006. The population density of the Reeve’s turtle, Chinemys reevesii, decreased markedly, from 279 turtles km⁻¹ in 2003 to 43 turtles km⁻¹ in 2006 in association with the artificial river alteration practices implemented by 2006. Low turtle population densities in other river sections where flood control measures have already been implemented suggest slow population recovery. River alteration practices also altered the age structures, sex ratios, and demographic characteristics of the turtle populations, although the exact consequences for population viability have not yet been determined. Because the turtles select concave submerged riverbanks or bottoms with slow or no current velocity, increased current velocity in the altered river section make the entire riverbank and bottom unsuitable for hibernation. Overall, river alteration for flood control during the winter season when turtles are inactive due to low water temperature negatively impacted freshwater turtle populations.     

Allometric scaling of lung volume and its consequences for marine turtle diving performance

Marine turtle lungs have multiple functions including respiration, oxygen storage and buoyancy regulation, so lung size is an important indicator of dive performance. We determined maximum lung volumes (V(L)) for 30 individuals from three species (Caretta caretta n=13; Eretmochelys imbricata n=12; Natator depressus n=5) across a range of body masses (M(b)): 0.9 to 46 kg. V(L) was 114 ml kg(-1) and increased with M(b) with a scaling factor of 0.92. Based on these values for V(L) we demonstrated that diving capacities (assessed via aerobic dive limits) of marine turtles were potentially over-estimated when the V(L)-body mass effect was not considered (by 10 to 20% for 5 to 25 kg turtles and by >20% for turtles > or =25 kg). While aerobic dive limits scale with an exponent of 0.6, an analysis of average dive durations in free-ranging chelonian marine turtles revealed that dive duration increases with a mass exponent of 0.51, although there was considerable scatter around the regression line. While this highlights the need to determine more parameters that affect the duration-body mass relationship, our results provide a reference point for calculating oxygen storage capacities and air volumes available for buoyancy control.     

Diving behavior in a free‐living,semi‐aquatic herbivore,the Eurasian beaver Castor fiber

Semi‐aquatic mammals have secondarily returned to the aquatic environment, although they spend a major part of their life operating in air. Moving both on land, as well as in, and under water is challenging because such species are considered to be imperfectly adapted to both environments. We deployed accelerometers combined with a depth sensor to study the diving behavior of 12 free‐living Eurasian beavers Castor fiber in southeast Norway between 2009 and 2011 to examine the extent to which beavers conformed with mass‐dependent dive capacities, expecting them to be poorer than wholly aquatic species. Dives were generally shallow (<1 m) and of short duration (<30 s), suggesting that the majority of dives were aerobic. Dive parameters such as maximum diving depth, dive duration, and bottom phase duration were related to the effort during different dive phases and the maximum depth reached. During the descent, mean vectorial dynamic body acceleration (VeDBA—a proxy for movement power) was highest near the surface, probably due to increased upthrust linked to fur‐ and lung‐associated air. Inconsistently though, mean VeDBA underwater was highest during the ascent when this air would be expected to help drive the animals back to the surface. Higher movement costs during ascents may arise from transporting materials up, the air bubbling out of the fur, and/or the animals’ exhaling during the bottom phase of the dive. In a manner similar to other homeotherms, beavers extended both dive and bottom phase durations with diving depth. Deeper dives tended to have a longer bottom phase, although its duration was shortened with increased VeDBA during the bottom phase. Water temperature did not affect diving behavior. Overall, the beavers’ dive profile (depth, duration) was similar to other semi‐aquatic freshwater divers. However, beavers dived for only 2.8% of their active time, presumably because they do not rely on diving for food acquisition.     

Diving behavior of immature hawksbill turtles (Eretmochelys imbricata) in a caribbean reef habitat

 Time-depth recorders were deployed on immature hawksbill turtles at the southwestern reefs of Mona Island, Puerto Rico, to examine patterns of diving behavior. Diving profiles of 10–12 day duration were obtained from five turtles ranging in carapace length from 27–52 cm. Turtles exhibited contrasting diurnal and nocturnal diving behaviors. During daylight hours, dives were made 92% of the time, featured continuous depth variation and were attributed to foraging activity. Foraging dive duration increased with turtle size; individual mean dive durations ranged from 19–26 min; mean post-dive surface intervals ranged from 37–64 s; mean depths ranged from 8–10 m. At night, dives were made 86% of the time to constant depths and were interpreted as resting behavior. Resting dive durations were not dependent on turtle size; individual mean dive durations ranged from 35–47 min; mean post-dive surface intervals ranged from 36–60 s; and mean depths from 7–10 m. Immature hawksbill turtles maintained short term home ranges several hundred meters in extension. Accepted: 2 July 1996     

Thermoconformity strategy in the freshwater turtle Hydromedusa tectifera (Testudines,Chelidae) in its southern distribution area

Ectotherm species are not capable of generating metabolic heat; therefore, they present different strategies for regulating their body temperatures, ranging from a precise degree of thermoregulation to a passive thermoconformity with ambient temperatures. In reptiles, aerial basking is the most common mechanism for gaining heat. However, among aquatic reptiles, such as freshwater turtles, aquatic basking is also frequent. Hydromedusa tectifera is a turtle of exclusively aquatic and nocturnal habits widely distributed in South America. We studied the relationship between body temperature (Tb) of H. tectifera and its habitat, and explored the effects of sex, life stage and body size and mass on Tb. Fieldwork was conducted in two streams of a mountain area of central Argentina. We recorded cloacal temperature, size and mass of 84 turtles. We also determined individuals’ sex and life stage (adult/juvenile). Regarding ambient temperatures, we measured water temperature on the surface (Tsurf) and at depth of turtle capture (Tdepth) and air temperature. Mean Tb was 18.58 °C (Min = 10.20 °C; Max = 25.70 °C). Tsurf and Tdepth were highly correlated. Multi-model analysis using Akaike criterion indicated that Tb was strongly associated with water temperature, whereas air temperature and body size and mass did not show a significant effect. There was also no effect of turtle sex or life stage on Tb. Our results indicate that H. tectifera is a thermoconformer and eurythermal species. A nocturnal pattern of activity and a fully aquatic lifestyle are suggested as determinant factors.     

The complete mitochondrial genome of the enigmatic bigheaded turtle (Platysternon): description of unusual genomic features and the reconciliation of phylogenetic hypotheses based on mitochondrial and nuclear DNA

Background  

The big-headed turtle (Platysternon megacephalum) from east Asia is the sole living representative of a poorly-studied turtle lineage (Platysternidae). It has no close living relatives, and its phylogenetic position within turtles is one of the outstanding controversies in turtle systematics. Platysternon was traditionally considered to be close to snapping turtles (Chelydridae) based on some studies of its morphology and mitochondrial (mt) DNA, however, other studies of morphology and nuclear (nu) DNA do not support that hypothesis.     

The physiology of diving in a north-temperate and three tropical turtle species

We examined changes in blood gases, plasma ions, and acid-base status during prolonged submergence (6 h) of four aquatic turtle species in aerated water at 20 °C. Our objective was to determine whether the temperate species, Chrysemys picta bellii, exhibits greater tolerance to submergence apnea than the tropical species, Pelomedusa subrufa, Elseya novaeguineae, and Emydura subglobosa. Blood was sampled from indwelling arterial catheters for measurements of blood PO₂, PCO₂, pH, and hematocrit and for plasma concentrations of lactate, glucose, Na⁺, K⁺, Cl⁻, total Ca, and total Mg. The pattern of change was similar in all species: a combined respiratory and metabolic acidosis associated with a marked decrease of blood PO₂. The severity of the acidosis developed in the temperate species, however, was significantly less than that of the tropical turtles. Lactate rose significantly and HCO₃ ⁻ fell proportionately in all turtles; changes in other plasma ion concentrations were small but were generally in the directions consistent with compensatory exchanges with other body compartments; i.e., cations (K⁺, Ca, and Mg increased) and anions (Cl⁻ decreased). The results indicate that hypoxia tolerance is a conserved trait in turtles, even in those that do not experience enforced winter submergence, and that the temperate species may be superior in this capacity because of reduced metabolic rate. Accepted: 3 March 1999     

Non‐marine turtle plays important functional roles in Indonesian ecosystems

The Southeast Asian box turtle (Cuora amboinensis) is numerically the most important turtle exported from Indonesia. Listed as Vulnerable by the IUCN, this turtle is heavily harvested and exported for food and traditional medicine in China and for the pet trade primarily in the United States, Europe, and Japan. Despite its significance in global markets, relatively little is known about the species’ ecology or importance to ecosystems. We conducted our research in a national park in Sulawesi, Indonesia, and our objectives were to quantify trophic breadth, capacity for seed dispersal between aquatic and terrestrial ecosystems, and whether ingestion of seeds by C. amboinensis enhances germination. We obtained diet samples from 200 individual turtles and found that the species is omnivorous, exhibiting an ontogenetic shift from more carnivorous to more omnivorous. Both subadults and adults scavenged on other vertebrates. In a seed passage experiment, turtles passed seeds for 2?9 days after ingestion. Radio‐tracked turtles moved, on average, about 35 m per day, indicating that seeds from ingested fruits, given seed passage durations, could be dispersed 70?313 m from the parent tree and potentially between wetland and upland ecosystems. In a seed germination experiment, we found that ingestion of seeds by turtles enhanced germination, as compared with control seeds, for four of six plant species tested. Of these, two are common in the national park, making up a significant proportion of plant biomass in lowland swamp forest and around ephemeral pools in savanna, and are highly valued outside of the park for their lumber for construction of houses, furniture, and boats. Protection of C. amboinensis populations may be important for maintaining trophic linkages that benefit biodiversity, communities, and local economies.