Aerobic Dives Research Articles

Diving deep into trouble: the role of foraging strategy and morphology in adapting to a changing environment.

Physiology places constraints on an animal's ability to forage and those unable to adapt to changing conditions may face increased challenges to reproduce and survive. As the global marine environment continues to change, small, air-breathing, endothermic marine predators such as otariids (fur seals and sea lions) and particularly females, who are constrained by central place foraging during breeding, may experience increased difficulties in successfully obtaining adequate food resources. We explored whether physiological limits of female otariids may be innately related to body morphology (fur seals vs sea lions) and/or dictate foraging strategies (epipelagic vs mesopelagic or benthic). We conducted a systematic review of the increased body of literature since the original reviews of Costa et al. (When does physiology limit the foraging behaviour of freely diving mammals? Int Congr Ser 2004;1275:359-366) and Arnould and Costa (Sea lions in drag, fur seals incognito: insights from the otariid deviants. In Sea Lions of the World Fairbanks. Alaska Sea Grant College Program, Alaska, USA, pp. 309-324, 2006) on behavioural (dive duration and depth) and physiological (total body oxygen stores and diving metabolic rates) parameters. We estimated calculated aerobic dive limit (cADL-estimated duration of aerobic dives) for species and used simulations to predict the proportion of dives that exceeded the cADL. We tested whether body morphology or foraging strategy was the primary predictor of these behavioural and physiological characteristics. We found that the foraging strategy compared to morphology was a better predictor of most parameters, including whether a species was more likely to exceed their cADL during a dive and the ratio of dive time to cADL. This suggests that benthic and mesopelagic divers are more likely to be foraging at their physiological capacity. For species operating near their physiological capacity (regularly exceeding their cADL), the ability to switch strategies is limited as the cost of foraging deeper and longer is disproportionally high, unless it is accompanied by physiological adaptations. It is proposed that some otariids may not have the ability to switch foraging strategies and so be unable adapt to a changing oceanic ecosystem.

Dive heart rate in harbour porpoises is influenced by exercise and expectations.

The dive response, a decrease in heart rate (fH) and peripheral vasoconstriction, is the key mechanism allowing breath-hold divers to perform long-duration dives. This pronounced cardiovascular response to diving has been investigated intensely in pinnipeds, but comparatively little is known for cetaceans, in particular in ecologically relevant settings. Here, we studied the dive fH response in one of the smallest cetaceans, the harbour porpoise (Phocoena phocoena). We used a novel multi-sensor data logger to record dive behaviour, fH, ventilations and feeding events in three trained porpoises, providing the first evaluation of cetacean fH regulation while performing a variety of natural behaviours, including prey capture. We predicted that tagged harbour porpoises would exhibit a decrease in fH in all dives, but the degree of bradycardia would be influenced by dive duration and activity, i.e. the dive fH response would be exercise modulated. In all dives, fH decreased compared with surface rates by at least 50% (mean maximum surface fH=173beatsmin-1, mean minimum dive fH=50beatsmin-1); however, dive fH was approximately 10beatsmin-1 higher in active dives as a result of a slower decrease in fH and more variable fH during pursuit of prey. We show that porpoises exhibit the typical breath-hold diver bradycardia during aerobic dives and that the fH response is modulated by exercise and dive duration; however, other variables such as expectations and individual differences are equally important in determining diving fH.

Exercise at depth alters bradycardia and incidence of cardiac anomalies in deep-diving marine mammals.

Unlike their terrestrial ancestors, marine mammals routinely confront extreme physiological and physical challenges while breath-holding and pursuing prey at depth. To determine how cetaceans and pinnipeds accomplish deep-sea chases, we deployed animal-borne instruments that recorded high-resolution electrocardiograms, behaviour and flipper accelerations of bottlenose dolphins (Tursiops truncatus) and Weddell seals (Leptonychotes weddellii) diving from the surface to >200 m. Here we report that both exercise and depth alter the bradycardia associated with the dive response, with the greatest impacts at depths inducing lung collapse. Unexpectedly, cardiac arrhythmias occurred in >73% of deep, aerobic dives, which we attribute to the interplay between sympathetic and parasympathetic drivers for exercise and diving, respectively. Such marked cardiac variability alters the common view of a stereotypic 'dive reflex' in diving mammals. It also suggests the persistence of ancestral terrestrial traits in cardiac function that may help explain the unique sensitivity of some deep-diving marine mammals to anthropogenic disturbances.

Why does the only ‘planktonic tetrapod’ dive? Determinants of diving behaviour in a marine ectotherm

Marine tetrapods represent powerful models for studying how evolutionary transitions shape the life history traits, physiology and behaviour of animals. Whereas adaptations to diving are driven primarily by the need to secure underwater food, diving in the pelagic sea snake, Hydrophis (Pelamis) platurus, seems less foraging-dependent. Indeed, this reptile captures fish while floating at the sea surface. Despite knowledge about its surface ecology, its underwater behaviour remains mostly unknown. Yet, study of this life phase is a key to understanding how and why this snake dives. In this study, we reanalysed published data on its diving behaviour. The pelagic sea snake spends 95% of its time underwater, where it can dive to 50 m and stay for 3.5 h without breathing. Dives are S-shaped, with a long phase of gradual ascent during which the snake is neutrally buoyant. Snake lungs deflate slowly during this phase at a rate that increases with water temperature, and thus metabolism. Dive duration is linked to inferred lung volume at the start of the dive, suggesting aerobic diving. We propose that pelagic sea snakes dive for multiple reasons, but primarily to avoid sea surface turbulence. Underwater, they can reduce metabolism by targeting cooler water layers. By hovering in the water column, they reduce energy expenditure and escape both surface and bottom predators, while more easily locating their own prey from underneath. Some marine turtles occasionally display S-shaped dives, but the role of such dives remains under debate. We suggest the study of sea snakes can help interpret diving behaviour in other lineages of marine reptiles. © 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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.

Aerobic dive limits of seals with mutant myoglobin using combined thermochemical and physiological data

This paper presents an integrated model of convective O2-transport, aerobic dive limits (ADL), and thermochemical data for oxygen binding to mutant myoglobin (Mb), used to quantify the impact of mutations in Mb on the dive limits of Weddell seals (Leptonychotes weddellii). We find that wild-type Mb traits are only superior under specific behavioral and physiological conditions that critically prolong the ADL, action radius, and fitness of the seals. As an extreme example, the mutations in the conserved His-64 reduce ADL up to 14±2min for routine aerobic dives, whereas many other mutations are nearly neutral in terms of ADL and the inferred fitness. We also find that the cardiac system, the muscle O2-store, animal behavior (i.e. pre-dive ventilation), and the oxygen binding affinity of Mb, KO2, have co-evolved to optimize dive duration at routine aerobic diving conditions, suggesting that such conditions are mostly selected upon in seals. The model is capable of roughly quantifying the physiological impact of single-protein mutations and thus bridges an important gap between animal physiology and molecular (protein) evolution.

The marine mammal dive response is exercise modulated to maximize aerobic dive duration

When aquatically adapted mammals and birds swim submerged, they exhibit a dive response in which breathing ceases, heart rate slows, and blood flow to peripheral tissues and organs is reduced. The most intense dive response occurs during forced submersion which conserves blood oxygen for the brain and heart, thereby preventing asphyxiation. In free-diving animals, the dive response is less profound, and energy metabolism remains aerobic. However, even this relatively moderate bradycardia seems diametrically opposed to the normal cardiovascular response (i.e., tachycardia and peripheral vasodilation) during physical exertion. As a result, there has been a long-standing paradox regarding how aquatic mammals and birds exercise while submerged. We hypothesized based on cardiovascular modeling that heart rate must increase to ensure adequate oxygen delivery to active muscles. Here, we show that heart rate (HR) does indeed increase with flipper or fluke stroke frequency (SF) during voluntary, aerobic dives in Weddell seals (HR=1.48SF-8.87) and bottlenose dolphins (HR=0.99SF+2.46), respectively, two marine mammal species with different evolutionary lineages. These results support our hypothesis that marine mammals maintain aerobic muscle metabolism while swimming submerged by combining elements of both dive and exercise responses, with one or the other predominating depending on the level of exertion.

Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle Myuchelys bellii 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 15days 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 (>3m) 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.

What Triggers the Aerobic Dive Limit? Patterns of Muscle Oxygen Depletion during Dives of Emperor Penguins

The concept that most dives are aerobic and less than the aerobic dive limit (the onset of post‐dive blood lactate accumulation) is a fundamental concept in diving physiology and the interpretation of diving behavior and foraging ecology. The physiological basis of the aerobic dive limit (ADL) is hypothesized to be depletion of the muscle O2 store. A dual‐wavelength near‐infrared spectrophotometer was developed and applied to the pectoral muscle to measure myoglobin O2 saturation levels during dives of emperor penguins (Aptenodytes forsteri) at an isolated dive hole on the sea ice of McMurdo Sound, Antarctica. Data revealed several patterns of O2 depletion. A monotonic decline to near complete O2 depletion during dives at the ADL occurred in some birds. Based on myoglobin concentration in the pectoral muscle and an assumption of no muscle blood flow, this corresponds to an O2 consumption rate of six to twelve ml O2 kg muscle−1 min−1. However, other birds demonstrated different O2 depletion patterns suggesting maintenance of some muscle perfusion during dives. Results support the hypothesis that the onset of post‐dive blood lactate accumulation is secondary to muscle O2 depletion during the dive but that the ADL may vary depending on muscle blood flow patterns. This research was supported by NSF grant OPP 0538594. CLW was supported by a NIH Marine Biotechnology Training Program Fellowship and a UC Regents Fellowship.

Surgical removal of right-to-left cardiac shunt in the American alligator(Alligator mississippiensis) causes ventricular enlargement but does not alter apnoea or metabolism during diving

Crocodilians have complete anatomical separation between the ventricles, similar to birds and mammals, but retain the dual aortic arch system found in all non-avian reptiles. This cardiac anatomy allows surgical modification that prevents right-to-left (R-L) cardiac shunt. A R-L shunt is a bypass of the pulmonary circulation and recirculation of oxygen-poor blood back to the systemic circulation and has often been observed during the frequent apnoeic periods of non-avian reptiles, particularly during diving in aquatic species. We eliminated R-L shunt in American alligators (Alligator mississippiensis) by surgically occluding the left aorta (LAo; arising from right ventricle) upstream and downstream of the foramen of Panizza (FoP), and we tested the hypotheses that this removal of R-L shunt would cause afterload-induced cardiac remodelling and adversely affect diving performance. Occlusion of the LAo both upstream and downstream of the FoP for approximately 21 months caused a doubling of RV pressure and significant ventricular enlargement (average approximately 65%) compared with age-matched, sham-operated animals. In a separate group of recovered, surgically altered alligators allowed to dive freely in a dive chamber at 23 degrees C, occlusion of the LAo did not alter oxygen consumption or voluntary apnoeic periods relative to sham animals. While surgical removal of R-L shunt causes considerable changes in cardiac morphology similar to aortic banding in mammals, its removal does not affect the respiratory pattern or metabolism of alligators. It appears probable that the low metabolic rate of reptiles, rather than pulmonary circulatory bypass, allows for normal aerobic dives.

Development of myoglobin concentration and acid buffering capacity in harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals from birth to maturity

Pinnipeds rely on muscle oxygen stores to help support aerobic diving, therefore muscle maturation may influence the behavioral ecology of young pinnipeds. To investigate the pattern of muscle development, myoglobin concentration ([Mb]) and acid buffering ability (beta) was measured in ten muscles from 23 harp and 40 hooded seals of various ages. Adult [Mb] ranged from 28-97 to 35-104 mg g tissue(-1) in harp and hooded seals, respectively, with values increasing from the cervical, non-swimming muscles to the main swimming muscles of the lumbar region. Neonatal and weaned pup muscles exhibited lower (approximately 30% adult values) and less variable [Mb] across the body than adults. In contrast, adult beta showed little regional variation (60-90 slykes), while high pup values (approximately 75% adult values) indicate significant in utero development. These findings suggest that intra-uterine conditions are sufficiently hypoxic to stimulate prenatal beta development, but that [Mb] development requires additional postnatal signal such as exercise, and/or growth factors. However, because of limited development in both beta and [Mb] during the nursing period, pups are weaned with muscles with lower aerobic and anaerobic capacities than those of adults.

Identification of foraging dives in free-ranging Weddell seals Leptonychotes weddellii: confirmation using video records

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 365:263-275 (2008) - DOI: https://doi.org/10.3354/meps07396 Identification of foraging dives in free-ranging Weddell seals Leptonychotes weddellii: confirmation using video records K. M. Madden1,*, L. A. Fuiman1, T. M. Williams2, R. W. Davis3 1Department of Marine Science, University of Texas at Austin, Marine Science Institute, 750 Channel View Drive, Port Aransas, Texas 78373, USA 2Department of Marine Biology, Texas A&M University, 5007 Avenue U, Galveston, Texas 77553, USA 3Department of Biology and Institute of Marine Science, EMS-A316, University of California, Santa Cruz, California 95064, USA *Email: kiersten.madden@mail.utexas.edu ABSTRACT: Understanding foraging behavior is important for addressing ecological questions about air-breathing marine vertebrates. However, the inability to directly observe them underwater has made it difficult to classify and understand their foraging behaviors. We equipped 8 free-ranging, adult Weddell seals with animal-borne video and data recorders (VDRs) to monitor their underwater behavior. Eighteen dive descriptors summarizing the duration, depth, speed, stroking frequency, gliding, and energetic cost of 234 dives were calculated. Dive descriptors were included in non-hierarchical cluster analyses that identified 5 groups of dives. Eight of the 18 dive descriptors contributed strongly to the discrimination between dive groups. Presence of prey on the video record confirmed Groups 1, 4, and 5 as foraging dives. Group 1 dives were deep and exceeded the estimated aerobic dive limit, while Group 4 dives were also deep but probably remained aerobic. Group 5 dives were shallow and aerobic. Comparisons with prior classifications showed that deep aerobic dives were similar in depth and duration to foraging dives identified in previous studies, but shallow aerobic dives represented a previously undescribed foraging category. Deep anaerobic dives also differed from previous classifications and were not indicative of benthic foraging, as was previously thought. The proportion of successful foraging dives (at least on prey encounter observed on video) varied among the groups and among locations with different bathymetry. The distribution of foraging dive types also varied among these locations. These results will help characterize foraging activity of Weddell seals and provide a better understanding of the energetic costs and foraging strategies of diving marine predators. KEY WORDS: Marine mammal · Behavior · Classification · Silverfish · Geographical variation · McMurdo Sound Full text in pdf format PreviousNextCite this article as: Madden KM, Fuiman LA, Williams T, Davis RW (2008) Identification of foraging dives in free-ranging Weddell seals Leptonychotes weddellii: confirmation using video records. Mar Ecol Prog Ser 365:263-275. https://doi.org/10.3354/meps07396 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 365. Online publication date: August 18, 2008 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2008 Inter-Research.

Size and distribution of oxygen stores in harp and hooded seals from birth to maturity

Pinnipeds rely primarily on oxygen stores in blood and muscles to support aerobic diving; therefore rapid development of body oxygen stores (TBO(2)) is crucial for pups to transition from nursing to independent foraging. Here, we investigate TBO(2) development in 45 harp (Pagophilus groenlandicus) and 46 hooded (Cystophora cristata) seals ranging in age from neonates to adult females. We found that hooded seal adults have the largest TBO(2) stores yet reported (89.5 ml kg(-1)), while harp seal adults have values more similar to other phocids (71.6 ml kg(-1)). In adults, large TBO(2) stores resulted from large blood volume (harp169, hood 194 ml kg(-1)) and high muscle Mb content (harp 86.0, hood 94.8 mg g(-1)). In contrast, pups of both species had significantly lower mass-specific TBO(2 )stores than adults, and stores declined rather than increased during the nursing period. This decline was due to a reduction in mass-specific blood volume and the absence of an increase in the low Mb levels (harp 21.0, hood 31.5 mg g(-1)). Comparisons with other phocid species suggests that the pattern of blood and muscle development in the pre- and post-natal periods varies with terrestrial period, and that muscle maturation rates may influence the length of the postweaning fast. However, final maturation of TBO(2) stores does not take place until after foraging begins.

The effect of myoglobin concentration on aerobic dive limit in a Weddell seal

One physiological adaptation for prolonged dive duration in marine mammals is an elevated myoglobin (Mb) concentration in skeletal muscle. To determine the influence of Mb concentration on the aerobic dive limit (ADL), we modified a previously published model that simulated aerobic dives in a Weddell seal (Leptonychotes weddellii) and ran it for four Mb concentrations: 5, 27, 54 and 108 g Mb kg(-1) muscle representing 7%, 50%, 100% and 200%, respectively, of the normal Mb concentration in Weddell seal skeletal muscle. The model was run at increasing levels of muscular exertion and under postabsorptive and postprandial conditions to determine their effect on ADL. For each set of conditions, the model was also run at different levels of cardiac output (i.e. the dive response was varied) to determine the level of convective oxygen transport that optimized the ADL. In a postabsorptive state at a routine level of muscular exertion for a diving Weddell seal, a decrease in Mb concentration to 7% of normal caused a 39% decrease in the ADL (18 min to 11 min), while doubling the Mb concentration increased the ADL by 30% (18 min to 24 min). Under postprandial conditions at a routine level of muscular exertion, doubling the Mb concentration did not increase the ADL (12 min). The convective oxygen transport needed to meet the metabolic demands (Heat Increment of Feeding, HIF) of the splanchnic organs during digestion and assimilation required a cardiac output that was not optimal for the efficient use of muscle oxygen stores. This resulted in an over perfusion of the muscles and incomplete use of myoglobin-bound oxygen. As a result, the postprandial ADL was limited by the amount of oxygen stored in the blood, and increasing the Mb concentration had no effect on the ADL. We hypothesize that myoglobin concentration is optimized for the type and duration of dives routinely made by Weddell seals, and that a further increase may not increase the ADL for most free-ranging dives.

Pharmacological blockade of the dive response: effects on heart rate and diving behaviour in the harbour seal (Phoca vitulina).

While diving, harbour seals (Phoca vitulina) manage their oxygen stores through cardiovascular adjustments, including bradycardia, a concurrent reduction in cardiac output, and peripheral vasoconstriction. At the surface, post-dive tachycardia facilitates rapid reloading of oxygen stores. Although harbour seals can tolerate >20 min of submergence, the majority of their natural dives are only 2-6 min and are usually followed by surface intervals that are <1 min, so they spend approximately 80% of their time submerged. Given that harbour seals meet their ecological needs through repetitive short aerobic dives, we were interested in the functional role, if any, of the dive response during these short dives. During voluntary diving in an 11 m deep tank, the cardiovascular responses to submergence of five harbour seals were manipulated using specific pharmacological antagonists, and the effects on diving behaviour were observed. Effects of pharmacological blockade on heart rate were also examined to assess the autonomic control of heart rate during voluntary diving. Heart rate was recorded using subcutaneous electrodes and data loggers, while diving behaviour was monitored using a video camera. The muscarinic blocker methoctramine blocked diving bradycardia, the alpha-adrenergic blocker prazosin blocked diving vasoconstriction, and the beta-adrenergic blocker metoprolol blocked post-dive tachycardia. Heart-rate analysis indicated that diving bradycardia is primarily modulated by the vagus, while post-dive tachycardia results from parasympathetic withdrawal as well as increased sympathetic stimulation of the heart. None of the pharmacological blockers had any effect on average dive or surface interval duration. Seals maintained a high percentage of time spent diving in all treatments. Thus, harbour seals do not appear to need the dive response during short dives in order to maintain an efficient dive strategy.

How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment

Although diving birds and mammals can withstand extended periods under water, field studies show that most perform mainly short, aerobic dives. Theoretical studies of diving have implicitly assumed that prey acquisition increases linearly with time spent searching and have examined strategies that maximize time spent foraging. We present a simple model of diving in seals, where dive durations are influenced by the seal's assessment of patch quality, but are ultimately constrained by oxygen balance. Prey encounters within a dive are assumed to be Poisson distributed and the scale of the patches is such that a predator will encounter a constant prey density during a dive. We investigated the effects of a simple giving-up rule, using recent prey encounter rate to assess patch quality. The model predicts that, for shallow dives, there should always be a net benefit from terminating dives early if no prey are encountered early in the dive. The magnitude of the benefit was highest at low patch densities. The relative gain depended on the magnitude of the travel time and the time taken to assess patch quality and the effect was reduced in deeper dives. As the time taken to decide decreased, the relative benefit increased, up to a maximum, but fell as decision time was reduced further. Frequency distributions of different aspects of dive durations from three deep-diving and two shallow-diving seal species are presented and compared with the model's predictions.

Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives.

Unlike their terrestrial counterparts, marine mammals stop breathing and reduce their convective oxygen transport while performing activities (e.g. foraging, courtship, aggressive interactions, predator avoidance and migration) that require sustained power output during submergence. Since most voluntary dives are believed to remain aerobic, the goal of this study was to examine the potential importance of the dive response in optimizing the use of blood and muscle oxygen stores during dives involving different levels of muscular exertion. To accomplish this, we designed a numerical model based on Fick's principle that integrated cardiac output (Vb), regional blood flow, convective oxygen transport (Q(O2)), muscle oxymyoglobin desaturation and regional rates of oxygen consumption (VO2). The model quantified how the optimal matching or mismatching of QO2 to VO2 affected the aerobic dive limit (ADL). We chose an adult Weddell seal Leptonycotes weddellii on which to base our model because of available data on the diving physiology and metabolism of this species. The results show that the use of blood and muscle oxygen stores must be completed at the same time to maximize the ADL for each level of VO2. This is achieved by adjusting Vb (range 19-94 % of resting levels) and muscle QO2 according to the rate of muscle oxygen consumption (VMO2). At higher values of VMO2, Vb and muscle perfusion must increase to maintain an appropriate QO2/VO2 ratio so that available blood and muscle oxygen stores are depleted at the same time. Although the dive response does not sequester blood oxygen exclusively for brain and heart metabolism during aerobic dives, as it does during forced submersion, a reduction in Vb and muscle perfusion below resting levels is necessary to maximize the ADL over the range of diving VO2 (approximately 2-9 ml O2 min-1 kg-1). Despite the reduction in Vb, convective oxygen transport is adequate to maintain aerobic metabolism and normal function in the splanchnic organs, kidneys and other peripheral tissues. As a result, physiological homeostasis is maintained throughout the dive. The model shows that the cardiovascular adjustments known as the dive response enable the diving seal to balance the conflicting metabolic demands of (1) optimizing the distribution and use of blood and muscle oxygen stores to maximize the ADL over the normal range of diving VO2 and (2) ensuring that active muscle receives adequate oxygen as VMO2 increases.

Diving and foraging patterns of Marbled Murrelets (Brachyramphus marmoratus): testing predictions from optimal-breathing models

The diving behavior of Marbled Murrelets (Brachyramphus marmoratus) was studied using telemetry along the Oregon coast during the 1995 and 1996 breeding seasons and examined in relation to predictions from optimal-breathing models. Duration of dives, pauses, dive bouts, time spent under water during dive bouts, and nondiving intervals between successive dive bouts were recorded. Most diving metrics differed between years but not with oceanographic conditions or shore type. There was no effect of water depth on mean dive time or percent time spent under water even though dive bouts occurred in depths from 3 to 36 m. There was a significant, positive relationship between mean dive time and mean pause time at the dive-bout scale each year. At the dive-cycle scale, there was a significant positive relationship between dive time and preceding pause time in each year and a significant positive relationship between dive time and ensuing pause time in 1996. Although it appears that aerobic diving was the norm, there appeared to be an increase in anaerobic diving in 1996. The diving performance of Marbled Murrelets in this study appeared to be affected by annual changes in environmental conditions and prey resources but did not consistently fit predictions from optimal-breathing models.

The Optimal Patch Use in Divers: Optimal Time Budget and the Number of Dive Cycles During Bout

Diving animals feeding on patchily distributed prey repeat dives with short surface intervals. For optimal foraging, they must optimally organize both the time budget and the number of dive cycles at a given patch. The cost of time and energy consumption per dive cycle is strongly affected by the respiratory metabolism used during dive because energetically efficient aerobic diving allows only a brief foraging duration during a dive whereas inefficient anaerobic diving allows a long foraging duration. I develop a model that predicts the effects of prey patch type on the optimal combination of time budget and the number of dive cycles by using the “marginal value theorem”. General features of the results are: (1) using anaerobic metabolism increases the range of prey patch types worth using in the habitat. (2) Anaerobic metabolism is favorable when the prey patch quality is high, the prey patch is situated in deep water, and the prey patch is hard to find, although the last one is not a strong condition. (3) When only aerobic diving is favorable, the time budget of the dive cycle is little affected by patch quality, but when anaerobic diving is favorable, it is strongly affected by patch quality. It is affected by patch depth in both cases. (4) When a dive bout is composed of many dive cycles, the dive duration and surface interval of the dive cycle are short. When long dive duration with long surface interval is optimal, the optimal number of dive cycles during the bout is small.

Physiology of diving of birds and mammals.

This review concentrates on the physiological responses, and their control, in freely diving birds and mammals that enable them to remain submerged and sometimes quite active for extended periods of time. Recent developments in technology have provided much detailed information on the behavior of these fascinating animals. Unfortunately, the advances in technology have been insufficient to enable physiologists to obtain anything like the same level of detail on the metabolic rate and physiological adjustments that occur during natural diving. This has led to much speculation and calculations based on many assumptions concerning usable oxygen stores and metabolic rate during diving, in an attempt to explain the observed behavior. Despite their shortcomings, these calculations have provided useful insights into the degree of adaptations of various species of aquatic birds and mammals. Many of them, e.g., ducks, smaller penguins, fur seals, and Weddell seals, seem able to metabolize aerobically, when diving, at approximately the same (if not greater) rate as they do at the surface. Their enhanced oxygen stores are able to support aerobic metabolism, at what would not be considered unusually low levels, for the duration of the dives, although there are probably circulatory readjustments to ensure that the oxygen stores are managed judiciously. For other species, such as the larger penguins, South Georgian shag, and female elephant seals, there is a general consensus that they must either be reducing their aerobic metabolic rate when diving, possibly by way of regional hypothermia, and/or producing ATP, at least partly, by anaerobiosis and metabolizing the lactic acid when at the surface (although this is hardly likely in the case of the female elephant seals). Circulation is the proximate regulator of metabolism during aerobic diving, and heart rate is the best single indicator of circulatory adjustment. During voluntary dives, heart rates range from extreme bradycardia to well above resting, reflecting metabolic performance. Efferent cardiac control is largely parasympathetic. Reflex cardiorespiratory responses are modulated by conditioning and habituation, but reflexes predominate during extended dives and during recovery, when gas exchange is maximized.