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 .     

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.     

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.     

The diving paradox: new insights into the role of the dive response in air-breathing vertebrates

When aquatic reptiles, birds and mammals submerge, they typically exhibit a dive response in which breathing ceases, heart rate slows, and blood flow to peripheral tissues is reduced. The profound dive response that occurs during forced submergence sequesters blood oxygen for the brain and heart while allowing peripheral tissues to become anaerobic, thus protecting the animal from immediate asphyxiation. However, the decrease in peripheral blood flow is in direct conflict with the exercise response necessary for supporting muscle metabolism during submerged swimming. In free diving animals, a dive response still occurs, but it is less intense than during forced submergence, and whole-body metabolism remains aerobic. If blood oxygen is not sequestered for brain and heart metabolism during normal diving, then what is the purpose of the dive response? Here, we show that its primary role may be to regulate the degree of hypoxia in skeletal muscle so that blood and muscle oxygen stores can be efficiently used. Paradoxically, the muscles of diving vertebrates must become hypoxic to maximize aerobic dive duration. At the same time, morphological and enzymatic adaptations enhance intracellular oxygen diffusion at low partial pressures of oxygen. Optimizing the use of blood and muscle oxygen stores allows aquatic, air-breathing vertebrates to exercise for prolonged periods while holding their breath.     

Breathing hypoxic gas affects the physiology as well as the diving behaviour of tufted ducks

We measured the effects of exposure to hypoxia (15% and 11% oxygen) and hypercapnia (up to 4.5% carbon dioxide) on rates of respiratory gas exchange both between and during dives in tufted ducks, Aythya fuligula, to investigate to what extent these may explain changes in diving behaviour. As found in previous studies, the ducks decreased dive duration (t(d)) and increased surface duration when diving from a hypoxic or hypercapnic gas mix. In the hypercapnic conditions, oxygen consumption during the dive cycle was not affected. Oxygen uptake between dives was reduced by only 17% when breathing a hypoxic gas mix of 11% oxygen. However, estimates of the rate of oxygen metabolism during the foraging periods of dives decreased nearly threefold in 11% oxygen. Given that tufted ducks normally dive well within their aerobic dive limits and that they significantly reduced their t(d) during hypoxia, it is not at all clear why they make this physiological adjustment.     

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.     

Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle <Emphasis Type="Italic">Myuchelys bellii</Emphasis> of eastern Australia

Freshwater turtles have an extraordinary physiological ability to endure dive times that can range from days to months using aquatic respiration. In cryptodires (e.g., white-lipped mud turtle Kinosternon leucostomum) aquatic respiration is via buccal or cutaneous routes whereas in pleurodires (e.g., Fitzroy River turtle Rheodytes leukops), it is achieved primarily via specialized cloacal bursae. This study records the voluntary diving performance of the western sawshelled turtle Myuchelys bellii in Bald Rock Creek from the temperate zone of the Murray–Darling Basin of Australia. Myuchelys bellii has a moderately specialized cloacal bursae morphology compared to other pleurodiran turtles and displays impressive dive durations spanning more than 15 days during the winter months. This is attributed to its ability to maintain aerobic dives via its cloacal bursae and low water temperatures in winter. Myuchelys bellii seasonal and diel diving performance, including its crepuscular habit, is comparable to R. leukops and Elseya albagula. This study also recorded the first aquatic hibernation at depth (>3 m) for any freshwater turtle; and only the second pleurodire to demonstrate aquatic hibernation as an overwintering strategy. Observed thermoregulation behavior in M. bellii is believed to provide multiple life history benefits.     

Hypoxia and interdemic variation in Poecilia latipinna

Variation in respiratory traits was quantified between two populations of the sailfin molly Poecilia latipinna (one from a periodically hypoxic salt marsh, Cedar Key, and one from a chronically normoxic river site, Santa Fe River). Two suites of characters were selected: traits that may show both short‐term acclimation response and interdemic variation in acclimation response (metabolic rate, critical oxygen tension and respiratory behaviour), and those that are not likely to respond to short‐term acclimation but may vary among populations (gill morphometric characters). Sailfin mollies from the salt marsh, acclimated to hypoxia (1 mg l⁻¹, c . 20 mmHg) for 6 weeks, spent less time conducting aquatic surface respiration and had lower gill ventilation rates than hypoxia‐acclimated conspecifics from the well‐oxygenated river site. Poecilia latipinna acclimated to hypoxia exhibited a lower critical oxygen tension ( P _c) than fish acclimated to normoxia; however, there was also a significant population effect. Poecilia latipinna from Cedar Key exhibited a lower P _c than fish from the Santa Fe River, regardless of acclimation. Cedar Key fish had a 14% higher mean gill surface area relative to fish from the Santa Fe River, a character that could account, at least in part, for their greater tolerance to hypoxia.     

The occurrence of aerial respiration in Rhinelepis strigosa during progressive hypoxia

Rhinelepis strigosa did not surface for air breathing in normoxic or moderate hypoxic water. This species initiated air breathing when the P _io₂ in the water reached 22 ± 1 mmHg. Once begun, the air-breathing frequency increased with decreasing P _io₂. Aquatic oxygen consumption was 21·0 ± 1·9ml O₂ kg⁻¹h⁻¹ in normoxic water, and was almost constant during progressive hypoxia until the P _io₂ reached 23·9 mmHg, considered the critical oxygen tension (P_co₂). Gill ventilation increased until close to the P _co₂ (7·9-fold) as a consequence of a greater increase in ventilatory volume than in breathing frequency. Gill oxygen extraction was 42 ± 5% and decreased with hypoxia, but under severe hypoxia returned to values characteristic of normoxic. The critical threshold for air breathing was coincident with the P_co₂ during aquatic respiration. This suggests that the air-breathing response is evoked by the aquatic oxygen tension at which the respiratory mechanisms fail to compensate for environmental hypoxia, and the gill O₂ uptake becomes insufficient to meet O₂ requirements.     

To what extent is the foraging behaviour of aquatic birds constrained by their physiology?

Aquatic birds have access to limited amounts of usable oxygen when they forage (dive) underwater, so the major physiological constraint to their behaviour is the need to periodically visit the water surface to replenish these stores and remove accumulated carbon dioxide. The size of the oxygen stores and the rate at which they are used (V dot o2) or carbon dioxide accumulates are the ultimate determinants of the duration that aquatic birds can remain feeding underwater. However, the assumption that the decision to terminate a dive is governed solely by the level of the respiratory stores is not always valid. Quantification of an optimal diving model for tufted ducks (Aythya fuligula) shows that while they dive efficiently by spending a minimum amount of time on the surface to replenish the oxygen used during a dive, they dive with nearly full oxygen stores and surface well before these stores are exhausted. The rates of carbon dioxide production during dives and removal during surface intervals are likely to be at least as important a constraint as oxygen; thus, further developments of optimal diving models should account for their effects. In the field, diving birds will adapt to changing environmental conditions and often maximise the time spent submerged during diving bouts. However, other factors influence the diving depths and durations of aquatic birds, and in some circumstances they are unable to forage sufficiently well to provide food for their offspring. The latest developments in telemetry have demonstrated how diving birds can make physiological decisions based on complex environmental factors. Diving penguins can control their inhaled air volume to match the expected depth, likely prey encounter rate, and buoyancy challenges of the following dive.     

The influence of temperature on diving behaviour in the alpine newt, Triturus alpestris

An aquatic lifestyle poses serious restriction to air-breathing animals in terms of time and energy spent during a dive cycle. The diving frequency increases with water temperature, therefore an ectotherm's time budget greatly depends on the thermal characteristics of the aquatic environment. Available data suggests that time costs caused by temperature-dependent dive frequency can be partially compensated for by adjusting the swimming speed and diving angle during dive cycle. We tested this prediction by examining the influence of temperature on the diving behaviour of the alpine newt, Triturus alpestris. The ascending speed and angle showed disparate patterns of temperature dependency, with a minor influence on travel duration. Surprisingly, at higher temperatures, the diving newts saved most of their time by restricting swimming activity in the water column during their return to the bottom and not by adjusting their ascending duration. Hence, aquatic newts have the capacity to reduce temperature-dependent time costs of aerial breathing primarily by behavioural modifications during the descending phase of the dive cycle.     

Metabolic adjustments of an air-breathing teleost, Channa maculata, to acute and prolonged exposure to hypoxic water

Plasma and tissue metabolite levels were measured in the air-breathing Channa maculata during acute and prolonged exposure to normoxic and hypoxic water. Exposure of the fish to hypoxic water (water oxygen partial pressure, PwO ₂= 50 mmHg) for 1 h caused increases in plasma glucose and lactate, liver and brain lactate, liver a-amino acid, heart and brain alanine and brain succinate levels. The metabolic changes in heart, brain and muscle could only be detected when Pw O₂ was 30 or 10 mmHg. Heart glycogen and liver lipid decreased during acute exposure. Prolonged exposure to hypoxic water ( Pw O₂= 30 mmHg) for 3 days caused an increase in plasma glycerol and liver lactate dehydrogenase activity, and a depletion of glycogen store in all tissues investigated. However, metabolite levels which had been elevated during acute hypoxic exposure were observed to return to their normoxic values after prolonged exposure. It was concluded that anaerobic metabolism was triggered by acute exposure to hypoxic water. Prolonged exposure to hypoxic water induced a metabolic readjustment involving mobilisation of lipid and glycogen stores, which is probably a reflection of the high metabolic load of aerial respiration imposed on the fish during exposure to hypoxic water.     

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.     

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.     

Buoyancy control in diving behavior of the loggerhead turtle,Caretta caretta

Neutral buoyancy at the stationary depth is advantageous for diving animals. The adjustment of the air inspiration before diving can be a mechanism of buoyancy control for diving animals with lungs. The stationary depth of neutral buoyancy becomes deeper with larger inspiration. Our aim was to examine whether the loggerhead sea turtle,Caretta caretta regulates the buoyancy to be neutral at the stationary depth of the dive. During an internesting period of the breeding season, we recorded the diving pattern of an adult female using a time-depth recorder and a time-swim distance recorder. The dives were classified into four types (Types 1 to 4) based on the time-depth profile. Types-3 and 4 (66% of the total dive duration) have three phases in each dive: (1) first descent, (2) gradual ascent (stationary period), and (3) final ascent. In the gradual ascent phase, the turtle stayed at a certain depth without swimming. This means that the turtle was neutrally buoyant during the gradual ascent phase. The depth of the gradual ascent phase was positively correlated with the dive duration, supporting the hypothesis that neutral buoyancy of the loggerhead turtle is achieved by the air in their lungs.     

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.     

Assessment of hypoxia avoidance behaviours in a eurythermal fish at two temperatures using a modified shuttlebox system

Behavioural avoidance responses of red drum (Sciaenops ocellatus) to aquatic hypoxia were investigated at 22 and 30°C using a modified shuttlebox system. Fish movement between a control side maintained at normoxia and a hypoxic side with stepwise decreasing water oxygen tension was analysed for entries into the hypoxic side, residence time per entry into the hypoxic side and total time in the hypoxic side. Acclimation to 30°C increased the oxygen threshold for the onset of hypoxia avoidance behaviours for entries and total time, while residence time per entry was unchanged.     

A review of the multi-level adaptations for maximizing aerobic dive duration in marine mammals: from biochemistry to behavior

Marine mammals exhibit multi-level adaptations, from cellular biochemistry to behavior, that maximize aerobic dive duration. A dive response during aerobic dives enables the efficient use of blood and muscle oxygen stores, but it is exercise modulated to maximize the aerobic dive limit at different levels of exertion. Blood volume and concentrations of blood hemoglobin and muscle myoglobin are elevated and serve as a significant oxygen store that increases aerobic dive duration. However, myoglobin is not homogeneously distributed in the locomotory muscles and is highest in areas that produce greater force and consume more oxygen during aerobic swimming. Muscle fibers are primarily fast and slow twitch oxidative with elevated mitochondrial volume densities and enhanced oxidative enzyme activities that are highest in areas that produce more force generation. Most of the muscle mitochondria are interfibriller and homogeneously distributed. This reduces the diffusion distance between mitochondria and helps maintain aerobic metabolism under hypoxic conditions. Mitochondrial volume densities and oxidative enzyme activities are also elevated in certain organs such as liver, kidneys, and stomach. Hepatic and renal function along with digestion and assimilation continue during aerobic dives to maintain physiological homeostasis. Most ATP production comes from aerobic fat metabolism in carnivorous marine mammals. Glucose is derived mostly from gluconeogenesis and is conserved for tissues such as red blood cells and the central nervous system. Marine mammals minimize the energetic cost of swimming and diving through body streamlining, efficient, lift-based propulsive appendages, and cost-efficient modes of locomotion that reduce drag and take advantage of changes in buoyancy with depth. Most dives are within the animal’s aerobic dive limit, which maximizes time underwater and minimizes recovery time at the surface. The result of these adaptations is increased breath-hold duration and enhanced foraging ability that maximizes energy intake and minimizes energy output while making aerobic dives to depth. These adaptations are the long, evolutionary legacy of an aquatic lifestyle that directly affects the fitness of marine mammal species for different diving abilities and environments.     

Surviving submerged—Setal tracheal gills for gas exchange in adult rheophilic diving beetles

The gas exchange in adult diving beetles (Coleoptera: Dytiscidae) relies on a subelytral air store, which has to be renewed in regular intervals at the water surface. The dive duration varies from a few minutes to 24 h depending on the species, activity, and temperature. However, some species remain submerged for several weeks. Stygobiont species do not ascend to the surface and gas exchange of these species remains unclear, but it is assumed that they require air filled voids for respiration or they use cutaneous respiration. In this study, we investigate the gas exchange in the running water diving beetle Deronectes aubei, which survive submerged for over 6 weeks. The diffusion distance through the cuticle is too great for cutaneous respiration. Therefore, the dissolved oxygen uptake of submerged beetles was determined and an oxygen uptake via the rich tracheated elytra was observed. Fine structure analyses (SEM and TEM) of the beetles showed tracheated setae mainly on the elytral surface, which acts as tracheal gills. Prevention of the air bubble formation at the tip of the abdomen, which normally act as physical gill in Dytiscidae, resulted in no effect in oxygen uptake in D. aubei, but this was the sole way for a submerged Hydroporus palustris to get oxygen. The setal gas exchange technique explains the restriction of D. aubei to rivers and brooks with high oxygen concentration and it may also be used by subterran living diving beetles, which lack access to atmospheric oxygen. The existence of setal tracheal gills in species in running water which are often found in the hyporheic zone and in stygobiont species supports the known evolution of stygobiont Dytiscidae from species of the hyporheic zone. For species in running water, setal tracheal gills could be seen as an adaptation to avoid drifting downstream by the current. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.