Diving behaviour of a reptile (Crocodylus johnstoni) in the wild: interactions with heart rate and body temperature

The differences in physical properties of air and water pose unique behavioural and physiological demands on semiaquatic animals. The aim of this study was to describe the diving behaviour of the freshwater crocodile Crocodylus johnstoni in the wild and to assess the relationships between diving, body temperature, and heart rate. Time-depth recorders, temperature-sensitive radio transmitters, and heart rate transmitters were deployed on each of six C. johnstoni (4.0-26.5 kg), and data were obtained from five animals. Crocodiles showed the greatest diving activity in the morning (0600-1200 hours) and were least active at night, remaining at the water surface. Surprisingly, activity pattern was asynchronous with thermoregulation, and activity was correlated to light rather than to body temperature. Nonetheless, crocodiles thermoregulated and showed a typical heart rate hysteresis pattern (heart rate during heating greater than heart rate during cooling) in response to heating and cooling. Additionally, dive length decreased with increasing body temperature. Maximum diving length was 119.6 min, but the greatest proportion of diving time was spent on relatively short (<45 min) and shallow (<0.4 m) dives. A bradycardia was observed during diving, although heart rate during submergence was only 12% lower than when animals were at the surface.     

Characteristics of the human cardiovascular system in the human diving response

Comparative-evolutional research of diving response showed that mechanisms of its expression had much in common in humans and in animals. Firstly, it involves a reflex bradycardia, vasoconstriction of peripheral vessels, and blood flow centralization. But, unlike animals whose diving response has some typical species peculiarities, human diving response is rather diverse. Four types of cardiovascular system response to face submersion were revealed: over-reactive, reactive, paradoxical, and nonreactive. These types were chosen according to the bradycardia character. It is also supposed that the occurrence of individual maximal R--R-interval, while serving as a signal to apnea stopping, is among the reasons of apnea activity limitation.     

A thorough and quantified method for classifying seabird diving behaviour

Time-depth recorders are commonly deployed on diving animals to obtain information on their aquatic behaviour. The recorded data provide a 2D profile of diving activity. As analyses of diving behaviour from such profiles have become more complex, these analyses have often suffered from a lack of consistency and rigour. There is a growing need for a simple, comparative method to classify diving behaviour thoroughly and quantitatively. Here, a new approach to the classification of the dive profiles of penguins is described, which probably has applicability for many other diving predators as well. This simple approach uses a small, coherent set of criteria to classify behaviours in a detailed and quantified manner, and with relative objectivity. Classification of diving behaviour is possible from the temporal scale of a wiggle within a dive to the scale of a bout of dives. The new method will make comparisons between species easier and clearer because these comparisons will be undertaken within a consistent, more objective framework.     

Potentially conflicting metabolic demands of diving and exercise in seals

Metabolic replacement rates (Ra) for glucose and free fatty acids (FFA) were determined during rest, exercise, and diving conditions in the gray seal using bolus injections of radiotracers. In the exercise experiments the seal swam at a metabolic rate elevated twofold over resting Ra for glucose and FFA while resting were similar to values found in terrestrial mammals and other marine mammal species. During exercise periods glucose turnover increased slightly while FFA turnover changes were variable. However, the energetic demands of exercise could not be met by the increase in the replacement rates of glucose or FFA even if both were completely oxidized. Under diving conditions the tracer pool displayed radically different specific activity curves indicative of the changes in perfusion and metabolic rate associated with a strong dive response. Since the radiotracer curves during exercise and diving differed qualitatively and quantitatively, it is possible that similar studies on freely diving animals can be used to assess the role of the diving response during underwater swimming in nature.     

Optimal diving behaviour for foraging in relation to body size

Overall, large animals dive longer and deeper than small animals; however, after the difference in body size is taken into account, smaller divers often tend to make relatively longer dives. Neither physiological nor theoretical explanations have been provided for this paradox. This paper develops an optimal foraging diving model to demonstrate the effect of body size on diving behaviour, and discusses optimal diving behaviour in relation to body size. The general features of the results are: (1) smaller divers should rely more heavily on anaerobic respiration, (2) larger divers should not always make longer dives than smaller divers, and (3) an optimal body size exists for each diving depth. These results explain the relatively greater diving ability observed in smaller divers, and suggest that if the vertical distribution of prey in the water column is patchy, there is opportunity for a population of diving animals to occupy habitat niches related to body size.     

Brain amino acid concentrations during diving and acid-base stress in turtles

To assess the role of brain amino acid neurotransmitters in the breath hold of diving animals, concentrations of free amino acids present in the brains of turtles immediately after 2 h of apneic diving (at 20 degrees C) were measured. Additionally, the same measurements were performed on four other groups of animals subjected to 2 h of hypercapnia (8% CO2 in air), anoxia (N2 breathing), anoxia plus hypercapnia (8% CO2-92% N2), or air breathing (control). Significant changes in the concentrations of the inhibitory amino acid neurotransmitters known to affect respiration [gamma-aminobutyric acid (GABA) and taurine] were seen. GABA increased significantly in those animals subjected to anoxia, whereas taurine decreased significantly in the diving animals and increased significantly in those subjected to anoxia plus hypercapnia. These results suggest that the attenuated central ventilatory drive during diving in these animals may be related to alterations in brain concentrations of GABA and taurine.     

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.     

Assessment of scale-dependent foraging behaviour in southern elephant seals incorporating the vertical dimension: a development of the First Passage Time method

1. Identifying the spatial scales at which top marine predators forage is important for understanding oceanic ecosystems. Several methods quantify how individuals concentrate their search effort along a given path. Among these, First-Passage Time (FPT) analysis is particularly useful to identify transitions in movement patterns (e.g. between searching and feeding). This method has mainly been applied to terrestrial animals or flying seabirds that have little or no vertical component to their foraging, so we examined the differences between classic FPT and a modification of this approach using the time spent at the bottom of a dive for characterizing the foraging activity of a diving predator: the southern elephant seal. 2. Satellite relayed data loggers were deployed on 20 individuals during three successive summers at the Kerguelen Islands, providing a total of 72 978 dives from eight juvenile males and nine adult females. 3. Spatial scales identified using the time spent at the bottom of a dive ( = 68.2 +/- 42.1 km) were smaller than those obtained by the classic FPT analysis ( = 104.7 +/- 67.3 km). Moreover, foraging areas identified using the new approach clearly overlapped areas where individuals increased their body condition, indicating that it accurately reflected the foraging activity of the seals. 4. These results suggest that incorporating the vertical dimension into FPT provides a different result to the surface path alone. Close to the Antarctic continent, within the pack-ice, sinuosity of the path could be explained by a high sea-ice concentration (restricting elephant seal movements), and was not necessarily related to foraging activity. 5. Our approach distinguished between actual foraging activity and changes in behaviour induced by the physical environment like sea ice, and could be applied to other diving predators. Inclusion of diving parameters appears to be essential to identify the spatial scale of foraging areas of diving animals.     

Training Rats to Voluntarily Dive Underwater: Investigations of the Mammalian Diving Response

Underwater submergence produces autonomic changes that are observed in virtually all diving animals. This reflexly-induced response consists of apnea, a parasympathetically-induced bradycardia and a sympathetically-induced alteration of vascular resistance that maintains blood flow to the heart, brain and exercising muscles. While many of the metabolic and cardiorespiratory aspects of the diving response have been studied in marine animals, investigations of the central integrative aspects of this brainstem reflex have been relatively lacking. Because the physiology and neuroanatomy of the rat are well characterized, the rat can be used to help ascertain the central pathways of the mammalian diving response. Detailed instructions are provided on how to train rats to swim and voluntarily dive underwater through a 5 m long Plexiglas maze. Considerations regarding tank design and procedure room requirements are also given. The behavioral training is conducted in such a way as to reduce the stressfulness that could otherwise be associated with forced underwater submergence, thus minimizing activation of central stress pathways. The training procedures are not technically difficult, but they can be time-consuming. Since behavioral training of animals can only provide a model to be used with other experimental techniques, examples of how voluntarily diving rats have been used in conjunction with other physiological and neuroanatomical research techniques, and how the basic training procedures may need to be modified to accommodate these techniques, are also provided. These experiments show that voluntarily diving rats exhibit the same cardiorespiratory changes typically seen in other diving animals. The ease with which rats can be trained to voluntarily dive underwater, and the already available data from rats collected in other neurophysiological studies, makes voluntarily diving rats a good behavioral model to be used in studies investigating the central aspects of the mammalian diving response.     

Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer

1. Foraging behaviours of the Australian sea lion (Neophoca cinerea) reflect an animal working hard to exploit benthic habitats. Lactating females demonstrate almost continuous diving, maximize bottom time, exhibit elevated field metabolism and frequently exceed their calculated aerobic dive limit. Given that larger animals have disproportionately greater diving capabilities, we wanted to examine how pups and juveniles forage successfully. 2. Time/depth recorders were deployed on pups, juveniles and adult females at Seal Bay Conservation Park, Kangaroo Island, South Australia. Ten different mother/pup pairs were equipped at three stages of development (6, 15 and 23 months) to record the diving behaviours of 51 (nine instruments failed) animals. 3. Dive depth and duration increased with age. However, development was slow. At 6 months, pups demonstrated minimal diving activity and the mean depth for 23-month-old juveniles was only 44 +/- 4 m, or 62% of adult mean depth. 4. Although pups and juveniles did not reach adult depths or durations, dive records for young sea lions indicate benthic diving with mean bottom times (2.0 +/- 0.2 min) similar to those of females (2.1 +/- 0.2 min). This was accomplished by spending higher proportions of each dive and total time at sea on or near the bottom than adults. Immature sea lions also spent a higher percentage of time at sea diving. 5. Juveniles may have to work harder because they are weaned before reaching full diving capability. For benthic foragers, reduced diving ability limits available foraging habitat. Furthermore, as juveniles appear to operate close to their physiological maximum, they would have a difficult time increasing foraging effort in response to reductions in prey. Although benthic prey are less influenced by seasonal fluctuations and oceanographic perturbations than epipelagic prey, demersal fishery trawls may impact juvenile survival by disrupting habitat and removing larger size classes of prey. These issues may be an important factor as to why the Australian sea lion population is currently at risk.     

Dangerous dive cycles and the proverbial ostrich

Data rarely are available to address the level of predation risk faced by diving animals in different parts of the water column. Consequently, most published research on diving behaviour implicitly assumes – like the proverbial ostrich – that 'unseen' predators are functionally unimportant. We argue that failure to consider diving in a predation risk framework may have precluded many insights into the ecology of aquatic foragers that breathe air. Using existing literature and a simple model, we suggest that fear from submerged predators in several systems might be influencing patch residence time, and therefore the duration of other dive cycle components. These analyses, along with an earlier model of predation risk faced by diving animals at the surface, suggest that dive cycle organisation can be modified to increase safety from predators, but only at the cost of reduced energy gain. Theoretical arguments presented here can seed hypotheses on factors contributing to population declines of diving species. For instance, adjustments to the dive cycle that reduce predation risk might be unaffordable if resources are scarce. Thus, if animals are to avoid imminent starvation or substantial loss of reproductive potential, resource declines might indirectly increase predation rates by limiting the extent to which dive cycles can deviate from those that would maximize energy gain. We hope that ideas presented in this paper stimulate other researchers to further develop theory and test predictions on how predation risk might influence diving behaviour and its ecological consequences.     

High diving metabolism results in a short aerobic dive limit for Steller sea lions (Eumetopias jubatus)

The diving capacity of marine mammals is typically defined by the aerobic dive limit (ADL) which, in lieu of direct measurements, can be calculated (cADL) from total body oxygen stores (TBO) and diving metabolic rate (DMR). To estimate cADL, we measured blood oxygen stores, and combined this with diving oxygen consumption rates (VO₂) recorded from 4 trained Steller sea lions diving in the open ocean to depths of 10 or 40 m. We also examined the effect of diving exercise on O₂ stores by comparing blood O₂ stores of our diving animals to non-diving individuals at an aquarium. Mass-specific blood volume of the non-diving individuals was higher in the winter than in summer, but there was no overall difference in blood O₂ stores between the diving and non-diving groups. Estimated TBO (35.9 ml O₂ kg^?1) was slightly lower than previously reported for Steller sea lions and other Otariids. Calculated ADL was 3.0 min (based on an average DMR of 2.24 L O₂ min^?1) and was significantly shorter than the average 4.4 min dives our study animals performed when making single long dives—but was similar to the times recorded during diving bouts (a series of 4 dives followed by a recovery period on the surface), as well as the dive times of wild animals. Our study is the first to estimate cADL based on direct measures of VO₂ and blood oxygen stores for an Otariid and indicates they have a much shorter ADL than previously thought.     

Structure of the endotheliocytes of cerebral vessels of aquatic mammals

By means of scanning microscopy the relief of luminal surface of endotheliocytes, lining microvessels of various parts of the brain in the Pusa sibirica, Phoca vitulina and Delphinapterus leucas have been studied. Specialized formations of the cellular surface--various processes, projections, toruli have been revealed; their character in various parts of the brain in diving animals is determined by the blood stream conditions and their different sensitivity to oxygen deficiency during diving. The peculiarities, revealed in the structure of the cerebral vessels intima, are considered as one manifestations of the adaptive properties in the organism of diving animals, which had been developed in them during the process of a long evolution, while they adapted to the aquatic environment.     

Dead or alive: The growing importance of shark diving in the Mid-Atlantic region

In the Mid-Atlantic Azores, the emergence of a seasonal ecotourism shark diving industry strongly contrasts with a North Atlantic shark fishery for regional, national and foreign fleets. Shark diving may provide an economic alternative to fishing, promoting an ecological and economical sustainable use of these animals, favouring their conservation. Understanding socio-economic aspects of this new Mid-Atlantic industry is the first step towards its sustainability and ultimately shark conservation. Data were collected by means of questionnaire designed to solicit information on shark divers’ knowledge, socio-economic status, expenditures and expectations, conducted between July and August 2014 on Pico and Faial Islands, to 144 divers. The majority of respondents were male (71%), between 25 and 40 years (41%), mainly from Germany, Holland and Austria, and 44% visited the Azores purposely to dive with sharks. On average, 2.6 sharks were seen per dive and 97% of respondents did not perceive any form of shark aggression or threat. The estimated generated income of shark diving in 2014 for the Azores amounts to 1,983.347€ (around US$2,244.890). Such an amount may easily increase following the current rates of expansion for (eco)tourism in the Azores and the infancy of the local shark diving activity. Finally, it is worth saying that nearly 70% of participants were willing to pay an extra amount until 60€ to ensure that shark diving remains an option and more than half (53%) would like to see that amount invested in conservation.     

Can diving-induced tissue nitrogen supersaturation increase the chance of acoustically driven bubble growth in marine mammals?

The potential for acoustically mediated causes of stranding in cetaceans (whales and dolphins) is of increasing concern given recent stranding events associated with anthropogenic acoustic activity. We examine a potentially debilitating non-auditory mechanism called rectified diffusion. Rectified diffusion causes gas bubble growth, which in an insonified animal may produce emboli, tissue separation and high, localized pressure in nervous tissue. Using the results of a dolphin dive study and a model of rectified diffusion for low-frequency exposure, we demonstrate that the diving behavior of cetaceans prior to an intense acoustic exposure may increase the chance of rectified diffusion. Specifically, deep diving and slow ascent/descent speed contributes to increased gas-tissue saturation, a condition that amplifies the likelihood of rectified diffusion. The depth of lung collapse limits nitrogen uptake per dive and the surface interval duration influences the amount of nitrogen washout from tissues between dives. Model results suggest that low-frequency rectified diffusion models need to be advanced, that the diving behavior of marine mammals of concern needs to be investigated to identify at-risk animals, and that more intensive studies of gas dynamics within diving marine mammals should be undertaken.     

Defining the limits of diving biochemistry in marine mammals

The field of marine mammal diving biochemistry was essentially untouched when Peter Hochachka turned his attention to it in the mid-1970s. Over the next 30 years, his work followed three main themes in this area: first, most biologists at that time supported the theory that diving mammals utilized enhanced metabolic pathways for hypoxic energy production (glycolysis to lactate) and reduced their metabolic rate while diving. Peter began his work on potential hypoxic adaptations in marine mammals by working out the details of how these pathways would be regulated. By the 1980s, he started to ask how diving mammals balanced the increased demands of exercise with the apparently conflicting demands to reduce aerobic metabolism while exercising underwater. By the 1990s, his work involved complex models of the interplay between the neural, hormonal, behavioral and evolutionary components of diving biochemistry and animal exercise. From a comparative approach, he excelled at bringing themes of hypoxic adaptation from many different types of animals to the field of diving mammal biochemistry. This review traces the history of Peter Hochachka's work on diving biochemistry from the perspective of those of us who spent time with him both inside the laboratory and outside in the field from Antarctica to Iceland.     

Microsphere studies of bullfrog central vascular shunts during diving and breathing in air.

Bidirectional central vascular shunts were measured during diving and breathing in air in unanesthetized bullfrogs by using pulmonary trapping of 38 mu mean diameter radionuclide-labelled microspheres. Six animals studied during diving exhibited a strong overall right-to-left shunting pattern comprised of both a predominant (68% mean) right-to-left shunt and a weak (23%) left-to-right countershunt. Five animals with access to air showed a variety of distribution patterns, including predominant shunts in the left-to-right (1 animal) and right-to-left (1 animal) directions, nearly complete mixing (2 animals) and separation of systemic and pulmonary venous returns (1 animal).     

Activity Budgets Derived From Time-Depth Recorders in a Diving Mammal

Abstract: We describe a method to convert continuously collected time-depth data from archival time-depth recorders (TDRs) into activity budgets for a benthic-foraging marine mammal. We used data from 14 TDRs to estimate activity-specific time budgets in sea otters (Enhydra lutris) residing near Cross Sound, southeast Alaska, USA. From the TDRs we constructed a continuous record of behavior for each individual over 39-46 days during summer of 1999. Behaviors were classified as foraging (diving to the bottom), other diving (traveling, grooming, interacting), and nondiving (assumed resting). The overall average activity budget (proportion of 24-hr/d) was 0.37 foraging (8.9 hr/d), 0.11 in other diving (2.6 hr/d), and 0.52 nondiving time (12.5 hr/d). We detected significant differences in activity budgets among individuals and between groups within our sample. Historically, the sea otter population in our study area had been expanding and sequentially reoccupying vacant habitat since their reintroduction to the area in the 1960s, and our study animals resided in 2 adjacent yet distinct locations. Males (n = 5) and individuals residing in recently occupied habitat (n = 4) spent 0.28-0.30 of their time foraging (6.7-7.2 hr/d), 0.17-0.18 of their time in other diving behaviors (4.1-4.3 hr/d), and 0.53-0.54 of their time resting (12.7-13.0 hr/d). In contrast, females (n = 9) and individuals residing in longer occupied habitat (n = 10) spent 0.40 of their time foraging (9.6 hr/d), 0.08-0.09 of their time in other diving behaviors (1.9-2.2 hr/d), and 0.51-0.52 of their time resting (12.2-12.5 hr/d). Consistent with these differences, sea otters residing in more recently occupied habitat captured more and larger clams (Saxidomus spp., Protothaca spp., Macoma spp., Mya spp., Clinocardium spp.) and other prey, and intertidal clams were more abundant and larger in this area. We found that TDRs provided data useful for measuring activity time budgets and behavior patterns in a diving mammal over long and continuous time periods. Fortuitous contrasts in time budgets between areas where our study animals resided suggest that activity time budgets estimated from TDRs may be a sensitive indicator of population status, particularly in relation to prey availability.     

The transition from day-to-night activity is a risk factor for the development of CNS oxygen toxicity in the diurnal fat sand rat (Psammomys obesus)

Performance and safety are impaired in employees engaged in shift work. Combat divers who use closed-circuit oxygen diving apparatus undergo part of their training during the night hours. The greatest risk involved in diving with such apparatus is the development of central nervous system oxygen toxicity (CNS-OT). We investigated whether the switch from day-to-night activity may be a risk factor for the development of CNS-OT using a diurnal animal model, the fat sand rat (Psammomys obesus). Animals were kept on a 12:12 light–dark schedule (6 a.m. to 6 p.m. at 500?lx). The study included two groups: (1) Control group: animals were kept awake and active during the day, between 09:00 and 15:00. (2) Experimental group: animals were kept awake and active during the night, between 21:00 and 03:00, when they were exposed to dim light in order to simulate the conditions prevalent during combat diver training. This continued for a period of 3?weeks, 5?days a week. On completion of this phase, 6-sulphatoxymelatonin (6-SMT) levels in urine were determined over a period of 24?h. Animals were then exposed to hyperbaric oxygen (HBO). To investigate the effect of acute melatonin administration, melatonin (50?mg/kg) or its vehicle was administered to the animals in both groups 20?min prior to HBO exposure. After the exposure, the activity of superoxide dismutase, catalase and glutathione peroxidase was measured, as were the levels of neuronal nitric oxide synthase (nNOS) and overall nitrotyrosylation in the cortex and hippocampus. Latency to CNS-OT was significantly reduced after the transition from day-to-night activity. This was associated with alterations in the level of melatonin metabolites secreted in the urine. Acute melatonin administration had no effect on latency to CNS-OT in either of the groups. Nevertheless, the activity of superoxide dismutase and catalase, as well as nitrotyrosine and nNOS levels, were altered in the hippocampus following melatonin administration. On the basis of these results, we suggest that a switch from diurnal to nocturnal activity may represent an additional risk factor for the development of CNS-OT. Utilizing a diurnal animal model may contribute to our understanding of the heightened risk of developing CNS-OT when diving with closed-circuit oxygen apparatus at night.     

A phylogenetic analysis of the allometry of diving

The oxygen store/usage hypothesis suggests that larger animals are able to dive for longer and hence deeper because oxygen storage scales isometrically with body mass, whereas oxygen usage scales allometrically with an exponent <1 (typically 0.67-0.75). Previous tests of the allometry of diving tend to reject this hypothesis, but they are based on restricted data sets or invalid statistical analyses (which assume that every species provides independent information). Here we apply information-theoretic statistical methods that are phylogenetically informed to a large data set on diving variables for birds and mammals to describe the allometry of diving. Body mass is strongly related to all dive variables except dive:pause ratio. We demonstrate that many diving variables covary strongly with body mass and that they have allometric exponents close to 0.33. Thus, our results fail to falsify the oxygen store/usage hypothesis. The allometric relationships for most diving variables are statistically indistinguishable for birds and mammals, but birds tend to dive deeper than mammals of equivalent mass. The allometric relationships for all diving variables except mean dive duration are also statistically indistinguishable for all major taxonomic groups of divers within birds and mammals, with the exception of the procellariiforms, which, strictly speaking, are not true divers.