Air-breathing Marine Vertebrates Research Articles

Conditioned Variation in Heart Rate During Static Breath-Holds in the Bottlenose Dolphin (Tursiops truncatus).

Previous reports suggested the existence of direct somatic motor control over heart rate (fH) responses during diving in some marine mammals, as the result of a cognitive and/or learning process rather than being a reflexive response. This would be beneficial for O2 storage management, but would also allow ventilation-perfusion matching for selective gas exchange, where O2 and CO2 can be exchanged with minimal exchange of N2. Such a mechanism explains how air breathing marine vertebrates avoid diving related gas bubble formation during repeated dives, and how stress could interrupt this mechanism and cause excessive N2 exchange. To investigate the conditioned response, we measured the fH-response before and during static breath-holds in three bottlenose dolphins (Tursiops truncatus) when shown a visual symbol to perform either a long (LONG) or short (SHORT) breath-hold, or during a spontaneous breath-hold without a symbol (NS). The average fH (ifHstart), and the rate of change in fH (difH/dt) during the first 20 s of the breath-hold differed between breath-hold types. In addition, the minimum instantaneous fH (ifHmin), and the average instantaneous fH during the last 10 s (ifHend) also differed between breath-hold types. The difH/dt was greater, and the ifHstart, ifHmin, and ifHend were lower during a LONG as compared with either a SHORT, or an NS breath-hold (P < 0.05). Even though the NS breath-hold dives were longer in duration as compared with SHORT breath-hold dives, the difH/dt was greater and the ifHstart, ifHmin, and ifHend were lower during the latter (P < 0.05). In addition, when the dolphin determined the breath-hold duration (NS), the fH was more variable within and between individuals and trials, suggesting a conditioned capacity to adjust the fH-response. These results suggest that dolphins have the capacity to selectively alter the fH-response during diving and provide evidence for significant cardiovascular plasticity in dolphins.

Thermoregulatory Strategies of Diving Air-Breathing Marine Vertebrates: A Review

The aquatic habitat of marine “air-breathing” vertebrates provides a significant thermoregulatory challenge due to the high thermal conductivity of water. In addition to temperature changes across their range, air-breathing vertebrates experience temperature changes on the timescale of seconds to minutes as they perform dives to access two critical resources: air at the surface and food at depth. In response to these challenges, air-breathing vertebrates have developed morphological and physiological adaptations that align with their life histories and phylogenies and contribute to homeostasis. However, the physiological and behavioral mechanisms used to maintain thermal balance while diving is still poorly understood. The cardiovascular system is integral to the physiological responses associated with the dive response, exercise, digestion, and thermoregulation. The adjustments required to meet one physiological demand may not be compatible with another and can result in a potential conflict between the various physiological demands imposed on air-breathing divers. We reviewed the literature on thermoregulation while diving in an effort to synthesize our current understanding of the thermoregulatory strategies of diving air-breathing marine vertebrates. Studies have demonstrated that thermoregulatory strategies can involve the temporal separation of two conflicting responses, a compromise in the performance of one response over another, or coordination of synergistic responses. We hope that a review and synthesis of both laboratory and field studies will stimulate future research efforts at the intersection of thermoregulation and diving physiology. Expanding the use of physiological biologgers, particularly to understudied species, will enhance our understanding of how these animals coordinate various physiological demands to maintain homeostasis in a thermally challenging environment.

Improving estimates of diving lung volume in air-breathing marine vertebrates.

The air volume in the respiratory system of marine tetrapods provides a store of O2 to fuel aerobic metabolism during dives; however, it can also be a liability, as the associated N2 can increase the risk of decompression sickness. In order to more fully understand the physiological limitations of different air-breathing marine vertebrates, it is therefore important to be able to accurately estimate the air volume in the respiratory system during diving. One method that has been used to do so is to calculate the air volume from glide phases - periods of movement during which no thrust is produced by the animal - which many species conduct during ascent periods, when gases are expanding owing to decreasing hydrostatic pressure. This method assumes that there is conservation of mass in the respiratory system, with volume changes only driven by pressure. In this Commentary, we use previously published data to argue that both the respiratory quotient and differences in tissue and blood gas solubility potentially alter the mass balance in the respiratory system throughout a dive. Therefore, near the end of a dive, the measured volume of gas at a given pressure may be 12-50% less than from the start of the dive; the actual difference will depend on the length of the dive, the cardiac output, the pulmonary shunt and the metabolic rate. Novel methods and improved understanding of diving physiology will be required to verify the size of the effects described here and to more accurately estimate the volume of gas inhaled at the start of a dive.

Pulmonary ventilation-perfusion mismatch: a novel hypothesis for how diving vertebrates may avoid the bends.

Hydrostatic lung compression in diving marine mammals, with collapsing alveoli blocking gas exchange at depth, has been the main theoretical basis for limiting N2 uptake and avoiding gas emboli (GE) as they ascend. However, studies of beached and bycaught cetaceans and sea turtles imply that air-breathing marine vertebrates may, under unusual circumstances, develop GE that result in decompression sickness (DCS) symptoms. Theoretical modelling of tissue and blood gas dynamics of breath-hold divers suggests that changes in perfusion and blood flow distribution may also play a significant role. The results from the modelling work suggest that our current understanding of diving physiology in many species is poor, as the models predict blood and tissue N2 levels that would result in severe DCS symptoms (chokes, paralysis and death) in a large fraction of natural dive profiles. In this review, we combine published results from marine mammals and turtles to propose alternative mechanisms for how marine vertebrates control gas exchange in the lung, through management of the pulmonary distribution of alveolar ventilation () and cardiac output/lung perfusion (), varying the level of in different regions of the lung. Man-made disturbances, causing stress, could alter the mismatch level in the lung, resulting in an abnormally elevated uptake of N2, increasing the risk for GE. Our hypothesis provides avenues for new areas of research, offers an explanation for how sonar exposure may alter physiology causing GE and provides a new mechanism for how air-breathing marine vertebrates usually avoid the diving-related problems observed in human divers.

Development of Dive Capacity in Northern Elephant Seals (Mirounga angustirostris): Reduced Body Reserves at Weaning Are Associated with Elevated Body Oxygen Stores during the Postweaning Fast.

Developmental increases in dive capacity have been reported in numerous species of air-breathing marine vertebrates. Previous studies in juvenile phocid seals suggest that increases in physiological dive capacity during the postweaning fast (PWF) are critical to support independent aquatic foraging. Although there is a strong relationship between size at weaning and PWF duration and body reserves at weaning vary considerably, few studies have considered whether such variation in body reserve magnitude promotes phenotypic modulation of dive capacity development during the PWF. Phenotypic modulation, a form of developmental plasticity in which rates and degrees of expression of the developmental program are modulated by environmental factors, may enhance diving capacity in weanlings with reduced PWF durations due to smaller body reserves at weaning if reduced body reserves promote accelerated development of dive capacity. We longitudinally measured changes in blood and muscle oxygen stores and muscle metabolic enzymes over the first 8 wk of the PWF in northern elephant seals and determined whether rates of change in these parameters varied with body reserves at weaning. We assessed whether erythropoietin (EPO), thyroid hormones, serum nonesterified fatty acid levels, and iron status influenced blood and muscle oxygen store development or were influenced by body reserves at weaning. Although mass-specific plasma volume and blood volume were relatively stable across the fast, both were elevated in animals with reduced body reserves. Surprisingly, hemoglobin and mean corpuscular hemoglobin concentrations declined over the PWF while hematocrit remained stable, and these variables were not associated with body reserves or EPO. Swimming muscle myoglobin and serum iron levels increased rapidly early in the PWF and were not related to body reserves. Patterns in maximal activities of muscle enzymes suggested a decline in total aerobic and anaerobic metabolic capacity over the PWF, despite maintenance of fat oxidation capacity. These results suggest that only development of blood volume is increased in smaller weanlings and that extended fasting durations in larger weanlings do not improve physiological dive capacity.

Decompression sickness ('the bends') in sea turtles.

Decompression sickness (DCS), as clinically diagnosed by reversal of symptoms with recompression, has never been reported in aquatic breath-hold diving vertebrates despite the occurrence of tissue gas tensions sufficient for bubble formation and injury in terrestrial animals. Similarly to diving mammals, sea turtles manage gas exchange and decompression through anatomical, physiological, and behavioral adaptations. In the former group, DCS-like lesions have been observed on necropsies following behavioral disturbance such as high-powered acoustic sources (e.g. active sonar) and in bycaught animals. In sea turtles, in spite of abundant literature on diving physiology and bycatch interference, this is the first report of DCS-like symptoms and lesions. We diagnosed a clinico-pathological condition consistent with DCS in 29 gas-embolized loggerhead sea turtles Caretta caretta from a sample of 67. Fifty-nine were recovered alive and 8 had recently died following bycatch in trawls and gillnets of local fisheries from the east coast of Spain. Gas embolization and distribution in vital organs were evaluated through conventional radiography, computed tomography, and ultrasound. Additionally, positive response following repressurization was clinically observed in 2 live affected turtles. Gas embolism was also observed postmortem in carcasses and tissues as described in cetaceans and human divers. Compositional gas analysis of intravascular bubbles was consistent with DCS. Definitive diagnosis of DCS in sea turtles opens a new era for research in sea turtle diving physiology, conservation, and bycatch impact mitigation, as well as for comparative studies in other air-breathing marine vertebrates and human divers.

Condition and mass impact oxygen stores and dive duration in adult female northern elephant seals

The range of foraging behaviors available to deep-diving, air-breathing marine vertebrates is constrained by their physiological capacity to breath-hold dive. We measured body oxygen stores (blood volume and muscle myoglobin) and diving behavior in adult female northern elephant seals, Mirounga angustirostris, to investigate age-related effects on diving performance. Blood volume averaged 74.4+/-17.0 liters in female elephant seals or 20.2+/-2.0% of body mass. Plasma volume averaged 32.2+/-7.8 liters or 8.7+/-0.7% of body mass. Absolute plasma volume and blood volume increased independently with mass and age. Hematocrit decreased weakly with mass but did not vary with age. Muscle myoglobin concentration, while higher than previously reported (7.4+/-0.7 g%), did not vary with mass or age. Pregnancy status did not influence blood volume. Mean dive duration, a proxy for physiological demand, increased as a function of how long seals had been at sea, followed by mass and hematocrit. Strong effects of female body mass (range, 218-600 kg) on dive duration, which were independent of oxygen stores, suggest that larger females had lower diving metabolic rates. A tendency for dives to exceed calculated aerobic limits occurred more frequently later in the at-sea migration. Our data suggest that individual physiological state variables and condition interact to determine breath-hold ability and that both should be considered in life-history studies of foraging behavior.

Foraging behaviour and habitat selection of the little penguin Eudyptula minor during early chick rearing in Bass Strait, Australia

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 366:293-303 (2008) - DOI: https://doi.org/10.3354/meps07507 Foraging behaviour and habitat selection of the little penguin Eudyptula minor during early chick rearing in Bass Strait, Australia Andrew J. Hoskins1,*, Peter Dann2, Yan Ropert-Coudert3, Akiko Kato4, André Chiaradia2, Daniel P. Costa5, John P. Y. Arnould1 1School of Life and Environmental Sciences, Deakin University, 221 Burwood Highway, Burwood, Victoria 3125, Australia 2Research Department, Phillip Island Nature Park, PO Box 97, Cowes, Victoria 3922, Australia 3Centre National de la Recherche Scientifique, Institut Pluridisciplinaire Hubert Curien, Département Ecologie, Physiologie et Ethologie, UMR 7178 CNRS-ULP, 23, rue Becquerel, 67087 Strasbourg Cedex 02, France 4National Institute of Polar Research, 1-9-10 Kaga, Itabashi-ku, Tokyo 173-8515, Japan 5Center for Ocean Health, University of California, 100 Shaffer Road, Santa Cruz, California 95060, USA *Email: ajhos@deakin.edu.au ABSTRACT: Knowledge of the foraging areas of top marine predators and the factors influencing them is central to understanding how their populations respond to environmental variability. While there is a large body of literature documenting the association of air-breathing marine vertebrates with areas of high marine productivity, there is relatively little information for species restricted to near-shore or continental-shelf areas. Differences in foraging range and diving behaviour of the little penguin Eudyptula minor were examined from 3 breeding colonies (Rabbit Island, Kanowna Island and Phillip Island) in central northern Bass Strait, southeast Australia, during the chick-guard stage using electronic tags (platform terminal transmitters, PTTs, and time-depth recorders, TDRs). Although there were large overall differences between individuals, the mean maximum foraging range (16.9 to 19.8 km) and mean total distance travelled (41.8 to 48.0 km) were similar between the 3 colonies, despite different bathymetric environments. Individuals from all 3 colonies selected foraging habitats within a narrow sea surface temperature (SST) range (16.0 to 16.4°C). While there were significant differences in mean dive depths (5.4 to 10.9 m) and mean durations (13.2 to 28.6 s) between the different colonies, the mean diving effort (vertical distance travelled: 936.3 to 964.3 m h–1) was similar. These findings suggest little penguins from the 3 colonies employ relatively similar foraging efforts yet are plastic in their foraging behaviours. KEY WORDS: Compositional analysis · Diving · Coastal ecosystem · Nearshore habitats · Sea surface temperature · Seabird Full text in pdf format PreviousNextCite this article as: Hoskins AJ, Dann P, Ropert-Coudert Y, Kato A, Chiaradia A, Costa DP, Arnould JPY (2008) Foraging behaviour and habitat selection of the little penguin Eudyptula minor during early chick rearing in Bass Strait, Australia. Mar Ecol Prog Ser 366:293-303. https://doi.org/10.3354/meps07507 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 366. Online publication date: August 29, 2008 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2008 Inter-Research.

Multiple foraging strategies in a marine apex predator, the Galapagos sea lion Zalophus wollebaeki

Three fundamental foraging patterns in air-breathing marine vertebrates have been described: epipelagic, mesopelagic and benthic. Many sea lion species with access to extensive con- tinental shelves have been described as benthic foragers. Coincidently these species are considered threatened. The Galapagos sea lion Zalophus wollebaeki, a top predator in the Galapagos Islands, is also considered threatened in this ecosystem. Sea lions at the central part of the archipelago have access to a vast continental shelf. For this reason we hypothesized that sea lions within this region would dive benthically. In addition, effective protection and conservation of this species requires knowledge of their foraging patterns and habitat utilization. We investigated the diving behaviour and habitat utilization of female Z. wollebaeki of a centrally located colony situated inside the high- est density area of the population using time-depth recorders and satellite telemetry. Three distinct foraging patterns were found and described (shallow, deep and bottom divers), and individuals uti- lizing each pattern foraged in different locations. Epipelagic, mesopelagic and benthic dives were exhibited in the sea lions' diving behaviour, but these dive types were not exclusively associated with a foraging pattern. Between foraging trips females hauled out more frequently on other islands than they did on their breeding colony. The finding of 3 distinct foraging patterns that differ spatially has direct implications for management, particularly with regard to fisheries interactions. Marine pro- tected areas can be implemented in the regions described as Z. wollebaeki foraging areas. Z. wolle- baeki's wide foraging range coupled with their use of multiple haul-out sites should be considered in future studies when determining foraging trip lengths and habitat utilization since presence/absence from the colony does not reflect foraging trip length.

Quantitative observations on marine mammals and reptiles of Kuwait’s Boubyan Island

Quantitative observations were recorded on air breathing marine vertebrates in the immediate vicinity of Boubyan Island from 17 February 2004 through 1 March 2005. In 398 hours of observation time during daylight, we made 159 sightings of Indo-Pacific Humpback Dolphins (Sousa chinensis) for a combined total of 524 individuals. We also recorded 38 individual seasnake (Hydrophis spp.) sightings. No marine turtles were observed during the study period. Pod size of the dolphins ranged from one to at least 30. Of the 159 sightings, 40% was comprised of a single individual, and 26% consisted of pairs. Pods of 10 or more members were observed on 13 occasions. Overall, we saw an average of 1.35 Sousa for each hour of observation time. Seasonal counts peaked in the spring with nearly 2 Sousa/h, and reached 3.3/h in April. Observation rates in the winter dipped to less than 0.7 Sousa/h. Khor Abdullah had the highest overall observation rate with 2.6 Sousa/h, and in the fall, this rate jumped to 4.3/h. In comparison, Hydrophis sea snakes were few with an overall observation rate of 0.1/h. This low number reflects the fact that sea snakes are present mostly in the summer, and are far less noticeable. Seasonal observation rates peaked in the summer with nearly 0.3/h and dipped to zero during the winter months. Sea snakes initially showed up in April when water temperature was just over 21ºC, and were no longer observed in November when water temperatures dropped from >20ºC in October to about 15ºC by December. Both Sousa and Hydrophis are relatively long-lived, apex species and could serve as environmental indicators for Boubyan Island’s planned development. Monitoring population abundances and tissues for contaminants is recommended.

Multiple foraging strategies in a marine apex predator, the Galapagos Sea Lion

Three fundamental foraging patterns in air-breathing marine vertebrates have been described: epipelagic, mesopelagic and benthic. Many sea lion species with access to extensive continental shelves have been described as benthic foragers. Coincidently these species are considered threatened. The Galapagos sea lion Zalophus wollebaeki, a top predator in the Galapagos Islands, is also considered threatened in this ecosystem. Sea lions at the central part of the archipelago have access to a vast continental shelf. For this reason we hypothesized that sea lions within this region would dive benthically. In addition, effective protection and conservation of this species requires knowledge of their foraging patterns and habitat utilization. We investigated the diving behaviour and habitat utilization of female Z. wollebaeki of a centrally located colony situated inside the highest density area of the population using time-depth recorders and satellite telemetry. Three distinct foraging patterns were found and described (shallow, deep and bottom divers), and individuals utilizing each pattern foraged in different locations. Epipelagic, mesopelagic and benthic dives were exhibited in the sea lions’ diving behaviour, but these dive types were not exclusively associated with a foraging pattern. Between foraging trips females hauled out more frequently on other islands than they did on their breeding colony. The finding of 3 distinct foraging patterns that differ spatially has direct implications for management, particularly with regard to fisheries interactions. Marine protected areas can be implemented in the regions described as Z. wollebaeki foraging areas. Z. wollebaeki’s wide foraging range coupled with their use of multiple haul-out sites should be considered in future studies when determining foraging trip lengths and habitat utilization since presence/absence from the colony does not reflect foraging trip length

A conceptual model of the variation in parental attendance in response to environmental fluctuation: foraging energetics of lactating sea lions and fur seals

1. A conceptual model is described and tested using empirical data that predicts how air-breathing marine vertebrates that are tied to shore for reproduction, but feed at sea, should respond to changes in prey availability. 2. The model examines the trade-off between changes in trip duration and foraging intensity as measured by field metabolic rate. It predicts that parents should increase the intensity of effort, and hence metabolic rate, prior to increasing the duration of foraging trips to maintain nutrient delivery to the young. 3. The model was tested with data on the foraging energetics and trip duration of four species, northern and Antarctic fur seals and California and Australian sea lions, each studied over two contrasting seasons. 4. The response of these marine predators to changes in prey availability due to climate driven environmental perturbation was found to support the conceptual model. Copyright © 2008 John Wiley & Sons, Ltd.

Vertical movements of North Sea cod

Various air-breathing marine vertebrates such as seals, turtles and seabirds show dis- tinct patterns of diving behaviour. For fish, the distinction between different vertical behaviours is often less clear-cut, as there are no surface intervals to differentiate between dives. Using data from acoustic tags (n = 23) and archival depth recorders attached to cod Gadus morhua (n = 92) in the southern North Sea, we developed a quantitative method of classifying vertical movements in order to facilitate an objective comparison of the behaviour of different individuals. This method expands the utilisation of data from data storage tags, with the potential for a better understanding of fish behaviour and enhanced individual based behaviour for improved ecosystem modelling. We found that cod were closely associated with the seabed for 90% of the time, although they showed distinct seasonal and spatial patterns in behaviour. For example, cod tagged in the southern North Sea exhib- ited high rates of vertical movement in spring and autumn that were probably associated with migra- tion, while the vertical movements of resident cod in other areas were much less extensive and were probably related to foraging or spawning behaviours. The full reasons underlying spatial and tempo- ral behavioural plasticity by cod in the North Sea warrant further investigation.

Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age

A defining physiological capability for air-breathing marine vertebrates is the amount of oxygen that can be stored in tissues and made available during dives. To evaluate the influence of oxygen storage capacity on aerobic diving capacity, we examined the extent to which blood and muscle oxygen stores varied as a function of age, body size and sex in the sexually dimorphic California sea lion, Zalophus californianus. We measured total body oxygen stores, including hematocrit, hemoglobin, MCHC, plasma volume, blood volume and muscle myoglobin in pups through adults of both sexes. Blood and muscle oxygen storage capacity was not fully developed by the end of the dependency period, with blood stores not fully developed until animals were larger juveniles (70 kg; 1.5-2.5 years) and muscle stores not until animals were sub-adult size (125 kg; 4-6 years). Differences in aerobic diving capacity among size classes were reflective of these major milestones in the development of oxygen stores. Male sea lions had greater absolute blood volume than females and reflected the larger mass of males, which became apparent when animals were large juveniles. Adult female sea lions had greater muscle myoglobin concentrations compared to males, resulting in greater mass-specific muscle and total oxygen stores. Delayed development of oxygen stores is consistent with the shallow epi-mesopelagic foraging behavior in this species. We hypothesize that the greater mass-specific oxygen stores of female sea lions compared to males is related to differences in foraging behavior between the sexes.

Blood nitrogen tensions of seals during simulated deep dives

Blood nitrogen tensions of seals during simulated deep dives