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Deep dives and high tissue density increase mean dive costs in California sea lions (Zalophus californianus)
Abstract
Diving is central to the foraging strategies of many marine mammals and seabirds. Still, the effect of dive depth on foraging cost remains elusive because energy expenditure is difficult to measure at fine temporal scales in wild animals. We used depth and acceleration data from 8 lactating California sea lions (Zalophus californianus) to model body density and investigate the effect of dive depth and tissue density on rates of energy expenditure. We calculated body density in 5 s intervals from the rate of gliding descent. We modeled body density across depth in each dive, revealing high tissue densities and diving lung volumes (DLV). DLV increased with dive depth in four individuals. We used buoyancy calculated from dive-specific body density models and drag calculated from swim speed to estimate metabolic power (W kg-1) and cost of transport (COT; J m-1 kg-1) in 5 s intervals during descents and ascents. Deeper dives required greater mean power for round-trip vertical transit, especially in individuals with higher tissue density. These trends likely follow from increased mean swim speed and buoyant hinderance that increasingly outweighs buoyant aid in deeper dives. This suggests deep diving is either a 'high cost, high reward' strategy or an energetically expensive option to access prey when shallow prey are limited, and that poor body condition may increase the energetic costs of deep diving. These results add to our mechanistic understanding of how foraging strategy and body condition affect energy expenditure in wild breath-hold divers.
Investigations of the molecular mechanisms behind detection of short, and particularly ultraviolet, wavelengths in arthropods have relied heavily on studies from insects due to the relative ease of heterologous expression of modified opsin proteins in model organisms like Drosophila. However, species outside of the Insecta can provide information on mechanisms for spectral tuning as well as the evolutionary history of pancrustacean visual pigments. Here we investigate the basis of spectral tuning in malacostracan short wavelength sensitive (SWS) opsins using phylogenetic comparative methods. Tuning sites that may be responsible for the difference between ultraviolet (UV) and violet visual pigment absorbance in the Malacostraca are identified, and the idea that an amino acid polymorphism at a single site is responsible for this shift is shown to be unlikely. Instead, we suggest that this change in absorbance is accomplished through multiple amino acid substitutions. On the basis of our findings, we conducted further surveys to identify spectral tuning mechanisms in the order Stomatopoda where duplication of UV opsins has occurred. Ancestral state reconstructions of stomatopod opsins from two main clades provide insight into the amino acid changes that lead to differing absorption by the visual pigments they form, and likely contribute the basis for the wide array of UV spectral sensitivities found in this order.
Management of gases during diving is not well understood across marine mammal species. Prior to diving, phocid (true) seals generally exhale, a behaviour thought to assist with the prevention of decompression sickness. Otariid seals (fur seals and sea lions) have a greater reliance on their lung oxygen stores, and inhale prior to diving. One otariid, the Antarctic fur seal ( Arctocephalus gazella ), then exhales during the final 50–85% of the return to the surface, which may prevent another gas management issue: shallow-water blackout. Here, we compare data collected from animal-attached tags (video cameras, hydrophones and conductivity sensors) deployed on a suite of otariid seal species to examine the ubiquity of ascent exhalations for this group. We find evidence for ascent exhalations across four fur seal species, but that such exhalations are absent for three sea lion species. Fur seals and sea lions are no longer genetically separated into distinct subfamilies, but are morphologically distinguished by the thick underfur layer of fur seals. Together with their smaller size and energetic dives, we suggest their air-filled fur might underlie the need to perform these exhalations, although whether to reduce buoyancy and ascent speed, for the avoidance of shallow-water blackout or to prevent other cardiovascular management issues in their diving remains unclear.
This article is part of the theme issue ‘Measuring physiology in free-living animals (Part I)’.
Quantifying metabolic rates and the factors that influence them is key to wildlife conservation efforts because anthropogenic activities and habitat alteration can disrupt energy balance, which is critical for reproduction and survival. We investigated the effect of diving behaviour, diet and season on field metabolic rates (FMR) and foraging success of lactating northern fur seals (Callorhinus ursinus) from the Pribilof Islands during a period of population decline. Variation in at-sea FMR was in part explained by season and trip duration, with values that ranged from 5.18 to 9.68 W kg-1 (n = 48). Fur seals experienced a 7.2% increase in at-sea FMR from summer to fall and a 1.9% decrease in at-sea FMR for each additional day spent at sea. There was no effect of foraging effort, dive depth or diet on at-sea FMR. Mass gains increased with trip duration and were greater in the fall compared with summer, but were unrelated to at-sea FMR, diving behaviour and diet. Seasonal increases in at-sea FMR may have been due to costs associated with the annual molt but did not appear to adversely impact the ability of females to gain mass on foraging trips. The overall high metabolic rates in conjunction with the lack of any diet-related effects on at-sea FMR suggests that northern fur seals may have reached a metabolic ceiling early in the population decline. This provides indirect evidence that food limitation may be contributing to the low pup growth rates observed in the Pribilof Islands, as a high metabolic overhead likely results in less available energy for lactation. The limited ability of female fur seals to cope with changes in prey availability through physiological mechanisms is particularly concerning given the recent and unprecedented environmental changes in the Bering Sea that are predicted to have ecosystem-level impacts.
How predators maximize energetic gains while minimizing the costs associated with exploiting heterogeneous prey remains a difficult ecological principle to test in natural systems.
Deep‐diving, air‐breathing predators face conflicting demands of oxygen conservation to extend dive time and oxygen usage from the exercise required to find and capture prey. How predators balance these opposing factors is additionally complicated by prey patches that are heterogeneous spatially, temporally and in quality.
Tags deployed on foraging fin whales revealed that deeper dives consisted of higher feeding rates (lunges/hr), as generally predicted by optimal foraging theory. By simultaneously measuring prey density and distribution in the local environment, we show that whales increased their dive depths in order to forage on the densest prey patches.
Despite the increased travel time needed to find deeper prey during a breath‐hold dive, the increase in feeding rates of fin whales and modelled prey consumption quadrupled compared to shallow foraging. Because the cost of transport is low at this extreme in body size, we posit that feeding on the deep prey patches significantly increases the energetic efficiency of foraging.
Given the increasing recognition that anthropogenic disturbance can curtail deep foraging dives in many cetacean species, endangered fin whales may be susceptible to significant energetic losses that may impact individual fitness and population health in some areas.
A free Plain Language Summary can be found within the Supporting Information of this article.
Many baleen whales undertake annual fasting and feeding cycles, resulting in substantial changes in their body condition, an important factor affecting fitness. As a measure of lipid-store body condition, tissue density of a few deep diving marine mammals has been estimated using a hydrodynamic glide model of drag and buoyancy forces. Here, we applied the method to shallow-diving humpback whales (Megaptera novaeangliae) in North Atlantic and Antarctic feeding aggregations. High-resolution 3-axis acceleration, depth and speed data were collected from 24 whales. Measured values of acceleration during 5 s glides were fitted to a hydrodynamic glide model to estimate unknown parameters (tissue density, drag term and diving gas volume) in a Bayesian framework. Estimated species-average tissue density (1031.6 ± 2.1 kg m⁻³, ±95% credible interval) indicates that humpback whale tissue is typically negatively buoyant although there was a large inter-individual variation ranging from 1025.2 to 1043.1 kg m⁻³. The precision of the individual estimates was substantially finer than the variation across different individual whales, demonstrating a progressive decrease in tissue density throughout the feeding season and comparably high lipid-store in pregnant females. The drag term (CDAm⁻¹) was estimated to be relatively high, indicating a large effect of lift-related induced drag for humpback whales. Our results show that tissue density of shallow diving baleen whales can be estimated using the hydrodynamic gliding model, although cross-validation with other techniques is an essential next step. This method for estimating body condition is likely to be broadly applicable across a range of aquatic animals and environments.
Foraging strategies and their resulting efficiency (energy gain to cost ratio) affect animals’ survival and reproductive success and can be linked to population dynamics. However, they have rarely been studied quantitatively in free-ranging animals. We investigated foraging strategies and efficiencies of wild northern fur seals Callorhinus ursinus during their breeding season to understand potential links to the observed population decline in the Bering Sea. We equipped 20 lactating females with biologgers to determine at-sea foraging behaviors. We measured energy expenditure while foraging using the doubly labeled water method, and energy gained using (1) the types and energy densities of prey consumed, and (2) the number of prey capture attempts (from acceleration data). Our results show that seals employed 2 foraging strategies. One group (40%) fed mostly in oceanic waters on small high energy-density prey, while the other (60%) stayed over the shallow continental shelf feeding mostly on larger, lower quality fish. Females foraging in oceanic waters captured 3 times more prey, and had double the foraging efficiencies of females that foraged on-shelf in neritic waters. However, neritic seals made comparatively shorter trips, and likely fed their pups ~20-25% more frequently. The presence of these strategies which either favor foraging efficiency (energy) or frequency of nursing (time) might be maintained in the population because they have similar net fitness outcomes. However, neither strategy appears to simultaneously maximise time and energy allocated to nursing, with potential impacts on the survival of pups during their first year at sea.
Intraspecific variability in foraging behavior has been documented across a range of taxonomic groups, yet the energetic consequences of this variation are not well understood for many species. Understanding the effect of behavioral variation on energy expenditure and acquisition is particularly crucial for mammalian carnivores because they have high energy requirements that place considerable pressure on prey populations. To determine the influence of behavior on energy expenditure and balance, we combined simultaneous measurements of at‐sea field metabolic rate (FMR) and foraging behavior in a marine carnivore that exhibits intraspecific behavioral variation, the California sea lion (Zalophus californianus). Sea lions exhibited variability in at‐sea FMR, with some individuals expending energy at a maximum of twice the rate of others. This variation was in part attributable to differences in diving behavior that may have been reflective of diet; however, this was only true for sea lions using a foraging strategy consisting of epipelagic (<200 m within the water column) and benthic dives. In contrast, sea lions that used a deep‐diving foraging strategy all had similar values of at‐sea FMR that were unrelated to diving behavior. Energy intake did not differ between foraging strategies and was unrelated to energy expenditure. Our findings suggest that energy expenditure in California sea lions may be influenced by interactions between diet and oxygen conservation strategies. There were no apparent energetic trade‐offs between foraging strategies, although there was preliminary evidence that foraging strategies may differ in their variability in energy balance. The energetic consequences of behavioral variation may influence the reproductive success of female sea lions and result in differential impacts of individuals on prey populations. These findings highlight the importance of quantifying the relationships between energy expenditure and foraging behavior in other carnivores for studies addressing fundamental and applied physiological and ecological questions.
To maximize foraging duration at depth, diving mammals are expected to use the lowest cost optimal speed during descent and ascent transit and to minimize the cost of transport by achieving neutral buoyancy. Here, we outfitted 18 deep-diving long-finned pilot whales with multi-sensor data loggers and found indications that their diving strategy is associated with higher costs than those of other deep-diving toothed whales. Theoretical models predict that optimal speed is proportional to (basal metabolic rate/drag)1/3 and therefore to body mass0.05. The transit speed of tagged animals (2.7±0.3 m s⁻¹) was substantially higher than the optimal speed predicted from body mass (1.4–1.7 m s⁻¹). According to the theoretical models, this choice of high transit speed, given a similar drag coefficient (median, 0.0035) to that in other cetaceans, indicated greater basal metabolic costs during diving than for other cetaceans. This could explain the comparatively short duration (8.9±1.5 min) of their deep dives (maximum depth, 444±85 m). Hydrodynamic gliding models indicated negative buoyancy of tissue body density (1038.8± 1.6 kg m–3, ±95% credible interval, CI) and similar diving gas volume (34.6±0.6 ml kg⁻¹, ±95% CI) to those in other deep-diving toothed whales. High diving metabolic rate and costly negative buoyancy imply a ‘spend more, gain more’ strategy of long-finned pilot whales, differing from that in other deep-diving toothed whales, which limits the costs of locomotion during foraging. We also found that net buoyancy affected the optimal speed: high transit speeds gradually decreased during ascent as the whales approached neutral buoyancy owing to gas expansion.
The depletion rate of the blood oxygen store, development of hypoxemia, and dive capacity are dependent on the distribution and rate of blood oxygen delivery to tissues while diving. Although blood oxygen extraction by working muscle would increase the blood oxygen depletion rate in a swimming animal, there is little information on the relationship between muscle workload and blood oxygen depletion during dives. Therefore, we examined flipper stroke rate, a proxy of muscle workload, and posterior vena cava oxygen profiles in four adult female California sea lions (Zalophus californianus) during foraging trips at sea. Flipper stroke rate analysis revealed that sea lions minimized muscle metabolism with a stroke-glide strategy when diving, and exhibited prolonged glides during the descent of deeper dives (> 100 m). During the descent phase of these deep dives, 55±21% of descent was spent gliding with the longest glides lasting over 160 s and covering a vertical distance of 340 m. Animals also consistently glided to the surface from 15-25 m depth during these deeper dives. Venous hemoglobin saturation (SvO2) profiles were highly variable throughout dives, with values occasionally increasing during shallow dives. The relationship between SvO2 and flipper stroke rate was weak during deeper dives, while this relationship was stronger during shallow dives. We conclude that 1) the depletion of oxygen in the posterior vena cava in deep diving sea lions is not dependent on stroke effort, and 2) stroke-glide patterns during dives contribute to a reduction of muscle metabolic rate.
Intraspecific variability is increasingly recognized as an important component of foraging behavior that can have implications for both population and community dynamics. We used an individual-level approach to describe the foraging behavior of an abundant, generalist predator that inhabits a dynamic marine ecosystem, focusing specifically on the different foraging strategies used by individuals in the same demographic group. We collected data on movements and diving behavior of adult female California sea lions (Zalophus californianus) across multiple foraging trips to sea. Sea lions (n = 35) used one of three foraging strategies that primarily differed in their oceanic zone and dive depth: a shallow, epipelagic strategy, a mixed epipelagic/benthic strategy, and a deep-diving strategy. Individuals varied in their degree of fidelity to a given strategy, with 66 % of sea lions using only one strategy on all or most of their foraging trips across the two-month tracking period. All foraging strategies were present in each of the sampling years, but there were inter-annual differences in the population-level importance of each strategy that may reflect changes in prey availability. Deep-diving sea lions traveled shorter distances and spent a greater proportion of time at the rookery than sea lions using the other two strategies, which may have energetic and reproductive implications. These results highlight the importance of an individual-based approach in describing the foraging behavior of female California sea lions and understanding how they respond to the seasonal and annual changes in prey avail-ability that characterize the California Current System.
Lipids and fatty acids (FA) were investigated in 4 species of forage fish: northern anchovy Engraulis mordax, Pacific sardine Sardinops sagax, Pacific herring Clupea pallasi, and whitebait smelt Allosmerus elongatus, for their ability to serve as biological indicators of ocean conditions in the California Current large marine ecosystem (CCLME). Samples were collected during the oceanographically contrasting years of 2005 and 2006. Upwelling was severely curtailed in the spring and early summer of 2005, leading to delayed biological productivity, whereas upwelling was relatively normal in spring 2006. Principal components analysis described 78% of the variance within the lipid and FA dataset using the first 2 principal components. We found significant intra- and interspecific, interannual, and seasonal differences in lipid and FA profiles using univariate and permutation- based multivariate analysis of variance. Indicator species analysis showed distinct lipid and FA properties associated with each fish species. Using the ratio of docosahexaenoic acid (C22:6n-3) to eicosapentaeonic acid (C20:5n-3), we detected a transition from a diet composed primarily of dinoflagellate origin in early 2005 to a diet resulting from diatom-based productivity by late summer 2006. This shift was due to interannual differences in primary production, which was confirmed through phytoplankton sampling. Our study demonstrates that lipid and FA biomarkers in the forage fish community can provide information on ocean conditions and productivity that affect food web structure in the CCLME.
Forces due to propulsion should approximate forces due to hydrodynamic drag for animals horizontally swimming at a constant speed with negligible buoyancy forces. Propulsive forces should also correlate with energy expenditures associated with locomotion-an important cost of foraging. As such, biologging tags containing accelerometers are being used to generate proxies for animal energy expenditures despite being unable to distinguish rotational movements from linear movements. However, recent miniaturizations of gyroscopes offer the possibility of resolving this shortcoming and obtaining better estimates of body accelerations of swimming animals. We derived accelerations using gyroscope data for swimming Steller sea lions (Eumetopias jubatus), and determined how well the measured accelerations correlated with actual swimming speeds and with theoretical drag. We also compared dive averaged dynamic body acceleration estimates that incorporate gyroscope data, with the widely used Overall Dynamic Body Acceleration (ODBA) metric, which does not use gyroscope data. Four Steller sea lions equipped with biologging tags were trained to swim alongside a boat cruising at steady speeds in the range of 4 to 10 kph. At each speed, and for each dive, we computed a measure called Gyro-Informed Dynamic Acceleration (GIDA) using a method incorporating gyroscope data with accelerometer data. We derived a new metric-Averaged Propulsive Body Acceleration (APBA), which is the average gain in speed per flipper stroke divided by mean stroke cycle duration. Our results show that the gyro-based measure (APBA) is a better predictor of speed than ODBA. We also found that APBA can estimate average thrust production during a single stroke-glide cycle, and can be used to estimate energy expended during swimming. The gyroscope-derived methods we describe should be generally applicable in swimming animals where propulsive accelerations can be clearly identified in the signal-and they should also prove useful for dead-reckoning and improving estimates of energy expenditures from locomotion.
Frequency of occurrence for the four most commonly identified prey species was 48.7% Pacific whiting Merluccius productus; 46.7% market squid Loligo opalescens; 35.9% rockfish Sebastes spp.; and 20.0% northern anchovy Engraulis mordax. California sea lions feed opportunistically on seasonally abundant schooling fishes and squids. -from AuthorsPacific whiting Merluccius productus market squid Loligo opalescens rockfish Sebastes northern anchovy Engraulis mordax
We examined the annual number of pups born, pup mortality, and pup weights of California sea lions (Zalophus californianus) at San Miguel Island, California, and related them to large and small-scale oceanographic indices in the central California Current System (CCS) between 1997 and 2011. Annual variability in the number of pups born and pup mortality was best explained by the mutlitvariate ENSO index (MEI) that tracks the El Niño/La Niña cycle. Annual variability in average pup weights was best explained by a sea surface temperature anomaly index (SSTA); average pup weights were lower in years when the SSTA was greater than 1 °C above normal. We demonstrated that California sea lions are sensitive to large and small-scale changes in ocean conditions through changes in their reproductive success, pup growth, and pup mortality. Therefore, California sea lions are an ideal indicator species for the IEA of the CCS.
We measured esophageal pressures, respiratory flow rates, and expired O2 and CO2 in six adult bottlenose dolphins (Tursiops truncatus) during voluntary breaths and maximal (chuff) respiratory efforts. The data were used to estimate the dynamic specific lung compliance (sCL), the O2 consumption rate (V̇O2 ) and CO2 production rates (V̇CO2 ) during rest. Our results indicate that bottlenose dolphins have the capacity to generate respiratory flow rates that exceed 130 l s(-1) and 30 l s(-1) during expiration and inspiration, respectively. The esophageal pressures indicated that expiration is passive during voluntary breaths, but active during maximal efforts, whereas inspiration is active for all breaths. The average sCL of dolphins was 0.31±0.04 cmH2O(-1), which is considerably higher than that of humans (0.08 cmH2O(-1)) and that previously measured in a pilot whale (0.13 cmH2O(-1)). The average estimated V̇O2 and V̇CO2 using our breath-by-breath respirometry system ranged from 0.857 to 1.185 l O2 min(-1) and 0.589 to 0.851 l CO2 min(-1), respectively, which is similar to previously published metabolic measurements from the same animals using conventional flow-through respirometry. In addition, our custom-made system allows us to approximate end tidal gas composition. Our measurements provide novel data for respiratory physiology in cetaceans, which may be important for clinical medicine and conservation efforts.
© 2015. Published by The Company of Biologists Ltd.
Diving animals modulate their swimming gaits to promote locomotor efficiency and so enable longer, more productive dives. Beaked whales perform extremely long and deep foraging dives that probably exceed aerobic capacities for some species. Here, we use biomechanical data from suction-cup tags attached to three species of beaked whales (Mesoplodon densirostris, N=10; Ziphius cavirostris, N=9; and Hyperoodon ampullatus, N=2) to characterize their swimming gaits. In addition to continuous stroking and stroke-and-glide gaits described for other diving mammals, all whales produced occasional fluke-strokes with distinctly larger dorso-ventral acceleration, which we termed 'type-B' strokes. These high-power strokes occurred almost exclusively during deep dive ascents as part of a novel mixed gait. To quantify body rotations and specific acceleration generated during strokes we adapted a kinematic method combining data from two sensors in the tag. Body rotations estimated with high-rate magnetometer data were subtracted from accelerometer data to estimate the resulting surge and heave accelerations. Using this method, we show that stroke duration, rotation angle and acceleration were bi-modal for these species, with B-strokes having 76% of the duration, 52% larger body rotation and four times more surge than normal strokes. The additional acceleration of B-strokes did not lead to faster ascents, but rather enabled brief glides, which may improve the overall efficiency of this gait. Their occurrence towards the end of long dives leads us to propose that B-strokes may recruit fast-twitch fibres that comprise ∼80% of swimming muscles in Blainville's beaked whales, thus prolonging foraging time at depth.
© 2015. Published by The Company of Biologists Ltd.
We examined structural properties of the marine mammal respiratory system, and tested Scholander's hypothesis that the chest is highly compliant by measuring the mechanical properties of the respiratory system in five species of pinniped under anesthesia (Pacific harbor seal, Phoca vitulina; northern elephant seal, Mirounga angustirostris; northern fur seal Callorhinus ursinus; California sea lion, Zalophus californianus; and Steller sea lion, Eumetopias jubatus). We found that the chest wall compliance (CCW) of all five species was greater than lung compliance (airways and alveoli, CL) as predicted by Scholander, which suggests that the chest provides little protection against alveolar collapse or lung squeeze. We also found that specific respiratory compliance was significantly greater in wild animals than in animals raised in an aquatic facility. While differences in ages between the two groups may affect this incidental finding, it is also possible that lung conditioning in free-living animals may increase pulmonary compliance and reduce the risk of lung squeeze during diving. Overall, our data indicate that compliance of excised pinniped lungs provide a good estimate of total respiratory compliance.
Foraging theory predicts that breath-hold divers adjust the time spent foraging at depth relative to the energetic cost of swimming, which varies with buoyancy (body density). However, the buoyancy of diving animals varies as a function of their body condition, and the effects of these changes on swimming costs and foraging behaviour have been poorly examined. A novel animal-borne accelerometer was developed that recorded the number of flipper strokes, which allowed us to monitor the number of strokes per metre swam (hereafter, referred to as strokes-per-metre) by female northern elephant seals over their months-long, oceanic foraging migrations. As negatively buoyant seals increased their fat stores and buoyancy, the strokes-per-metre increased slightly in the buoyancy-aided direction (descending), but decreased significantly in the buoyancy-hindered direction (ascending), with associated changes in swim speed and gliding duration. Overall, the round-trip strokes-per-metre decreased and reached a minimum value when seals achieved neutral buoyancy. Consistent with foraging theory, seals stayed longer at foraging depths when their round-trip strokes-per-metre was less. Therefore, neutrally buoyant divers gained an energetic advantage via reduced swimming costs, which resulted in an increase in time spent foraging at depth, suggesting a foraging benefit of being fat.
California sea lions increased from approximately 50 000 to
340 000 animals in the last 40 years, and their pups are
starving and stranding on beaches in southern California,
raising questions about the adequacy of their food supply. We
investigated whether the declining sea lion pup weight at San
Miguel rookery was associated with changes in abundance
and quality of sardine, anchovy, rockfish and market squid
forage. In the last decade off central California, where breeding
female sea lions from San Miguel rookery feed, sardine and
anchovy greatly decreased in biomass, whereas market squid
and rockfish abundance increased. Pup weights fell as forage
food quality declined associated with changes in the relative
abundances of forage species. A model explained 67% of
the variance in pup weights using forage from central and
southern California and 81% of the variance in pup weights
using forage from the female sea lion foraging range. A shift
from high to poor quality forage for breeding females results
in food limitation of the pups, ultimately flooding animal
rescue centres with starving sea lion pups. Our study is
unusual in using a long-term, fishery-independent dataset to
directly address an important consequence of forage decline
on the productivity of a large marine predator. Whether
forage declines are environmentally driven, are due to a
combination of environmental drivers and fishing removals,
or are due to density-dependent interactions between forage
and sea lions is uncertain. However, declining forage abundance
and quality was coherent over a large area (32.5–38◦ N) for a decade,
suggesting that trends in forage are environmentally driven.
Pumas (Puma concolor) live in diverse, often rugged, complex habitats. The energy they expend for hunting must account for this complexity but
is difficult to measure for this and other large, cryptic carnivores. We developed and deployed a physiological SMART (species movement, acceleration, and radio tracking) collar that used accelerometry to continuously monitor energetics, movements, and behavior of free-ranging pumas. This felid species displayed marked individuality in predatory activities, ranging from low-cost sit-and-wait behaviors to constant movements with energetic costs averaging 2.3 times those predicted for running mammals. Pumas reduce these costs by remaining cryptic and precisely matching maximum pouncing force (overall dynamic body acceleration = 5.3 to 16.1g) to prey size. Such instantaneous energetics help to explain why most felids stalk and pounce, and their analysis represents a powerful approach for accurately forecasting resource demands required for survival by large, mobile predators.
To be successful, marine predators must alter their foraging behavior in response to changes in their environment. To understand the impact and severity of environmental change on a population it is necessary to first describe typical foraging patterns and identify the underlying variability that exists in foraging behavior. Therefore, we characterized the at-sea behavior of adult female California sea lions (n = 32) over three years (2003, 2004, and 2005) using satellite transmitters and time-depth recorders and examined how foraging behavior varied among years. In all years, sea lions traveled on average 84.7 ± 11.1 km from the rookery during foraging trips that were 3.2 ± 0.3 d. Sea lions spent 42.7% ± 1.9% of their time at sea diving and displayed short (2.2 ± 0.2 min), shallow dives (58.5 ± 8.5 m). Among individuals, there was significant variation in both dive behavior and movement patterns, which was found in all years. Among years, differences were found in trip durations, distances traveled, and some dive variables (e.g., dive duration and bottom time) as sea lions faced moderate variability in their foraging habitat (increased sea-surface temperatures, decreased upwelling, and potential decreased prey abundance). The flexibility we found in the foraging behavior of California sea lions may be a mechanism to cope with environmental variability among years and could be linked to the continuing growth of sea lion populations.
Sea otters (Enhydra lutris) have the highest mass-specific metabolic rate of any marine mammal, which is superimposed on the inherently high costs of reproduction and lactation in adult females. These combined energetic demands have been implicated in the poor body condition and increased mortality of female sea otters nearing the end of lactation along the central California coast. However, the cost of lactation is unknown and currently cannot be directly measured for this marine species in the wild. Here, we quantified the energetic demands of immature sea otters across five developmental stages as a means of assessing the underlying energetic challenges associated with pup rearing that may contribute to poor maternal condition. Activity-specific metabolic rates, daily activity budgets and field metabolic rates (FMR) were determined for each developmental stage. Mean FMR of pre-molt pups was 2.29±0.81 MJ day(-1) and increased to 6.16±2.46 and 7.41±3.17 MJ day(-1) in post-molt pups and dependent immature animals, respectively. Consequently, daily energy demands of adult females increase 17% by 3 weeks postpartum and continue increasing to 96% above pre-pregnancy levels by the average age of weaning. Our results suggest that the energetics of pup rearing superimposed on small body size, marine living and limited on-board energetic reserves conspire to make female sea otters exceptionally vulnerable to energetic shortfalls. By controlling individual fitness, maternal behavior and pup provisioning strategies, this underlying metabolic challenge appears to be a major factor influencing current population trends in southern sea otters (Enhydra lutris nereis).
Heart rate and peripheral blood flow distribution are the primary determinants of the rate and pattern of oxygen store utilisation and ultimately breath-hold duration in marine endotherms. Despite this, little is known about how otariids (sea lions and fur seals) regulate heart rate (fH) while diving. We investigated dive fH in five adult female California sea lions (Zalophus californianus) during foraging trips by instrumenting them with digital electrocardiogram (ECG) loggers and time depth recorders. In all dives, dive fH (number of beats/duration; 50±9 beats min(-1)) decreased compared with surface rates (113±5 beats min(-1)), with all dives exhibiting an instantaneous fH below resting (<54 beats min(-1)) at some point during the dive. Both dive fH and minimum instantaneous fH significantly decreased with increasing dive duration. Typical instantaneous fH profiles of deep dives (>100 m) consisted of: (1) an initial rapid decline in fH resulting in the lowest instantaneous fH of the dive at the end of descent, often below 10 beats min(-1) in dives longer than 6 min in duration; (2) a slight increase in fH to ~10-40 beats min(-1) during the bottom portion of the dive; and (3) a gradual increase in fH during ascent with a rapid increase prior to surfacing. Thus, fH regulation in deep-diving sea lions is not simply a progressive bradycardia. Extreme bradycardia and the presumed associated reductions in pulmonary and peripheral blood flow during late descent of deep dives should (a) contribute to preservation of the lung oxygen store, (b) increase dependence of muscle on the myoglobin-bound oxygen store, (c) conserve the blood oxygen store and (d) help limit the absorption of nitrogen at depth. This fH profile during deep dives of sea lions may be characteristic of deep-diving marine endotherms that dive on inspiration as similar fH profiles have been recently documented in the emperor penguin, another deep diver that dives on inspiration.
The management and depletion of O2 stores underlie the aerobic dive capacities of marine mammals. The California sea lion (Zalophus californianus) presumably optimizes O2 store management during all dives, but approaches its physiological limits during deep dives to greater than 300 m depth. Blood O2 comprises the largest component of total body O2 stores in adult sea lions. Therefore, we investigated venous blood O2 depletion during dives of California sea lions during maternal foraging trips to sea by: (1) recording venous partial pressure of O2 (PO2) profiles during dives, (2) characterizing the O2-hemoglobin (Hb) dissociation curve of sea lion Hb and (3) converting the PO2 profiles into percent Hb saturation (SO2) profiles using the dissociation curve. The O2-Hb dissociation curve was typical of other pinnipeds (P50=28±2 mmHg at pH 7.4). In 43% of dives, initial venous SO2 values were greater than 78% (estimated resting venous SO2), indicative of arterialization of venous blood. Blood O2 was far from depleted during routine shallow dives, with minimum venous SO2 values routinely greater than 50%. However, in deep dives greater than 4 min in duration, venous SO2 reached minimum values below 5% prior to the end of the dive, but then increased during the last 30-60 s of ascent. These deep dive profiles were consistent with transient venous blood O2 depletion followed by partial restoration of venous O2 through pulmonary gas exchange and peripheral blood flow during ascent. These differences in venous O2 profiles between shallow and deep dives of sea lions reflect distinct strategies of O2 store management and suggest that underlying cardiovascular responses will also differ.
Flying and terrestrial animals should spend energy to move while supporting their weight against gravity. On the other hand, supported by buoyancy, aquatic animals can minimize the energy cost for supporting their body weight and neutral buoyancy has been considered advantageous for aquatic animals. However, some studies suggested that aquatic animals might use non-neutral buoyancy for gliding and thereby save energy cost for locomotion. We manipulated the body density of seals using detachable weights and floats, and compared stroke efforts of horizontally swimming seals under natural conditions using animal-borne recorders. The results indicated that seals had smaller stroke efforts to swim a given speed when they were closer to neutral buoyancy. We conclude that neutral buoyancy is likely the best body density to minimize the cost of transport in horizontal swimming by seals.
The African wild dog Lycaon pictus is critically endangered, with only about 5,000 animals remaining in the wild(1). Across a range of habitats, there is a negative relationship between the densities of wild dogs and of the spotted hyaena Crocuta crocuta(2). It has been suggested that this is because hyaenas act as 'kleptoparasites' and steal food from dogs. We have now measured the daily energy expenditure of free-ranging dogs to model the impact of kleptoparasitism on energy balance, The daily energy expenditures of six dogs, measured by the doubly labelled water technique, averaged 15.3 megajoules per day. We estimated that the instantaneous cost of hunting was twenty-five times basal metabolic rate. As hunting is energetically costly, a small loss of food to kleptoparasites has a large impact on the amount of time that dogs must hunt to achieve energy balance. They normally hunt for around 3.5 hours per day but need to increase this to 12 hours if they lose 25% of their food. This would increase th
SYNOPSIS. The evolution of fully aquatic mammals from quadrupedal, terrestrial mammals was associated with changes in morphology and swimming mode. Drag is minimized by streamlining body shape and appendages. Improvement in speed, thrust production and efficiency is accomplished by a change of swimming mode. Terrestrial and semiaquatic mammals employ drag-based propulsion with paddling appendages, whereas fully aquatic mammals use lift-based propulsion with oscillating hydrofoils. Aerobic efficiencies are low for drag-based swimming, but reach a maximum of 30% for lift-based propulsion. Propulsive efficiency is over 80% for lift-based swimming while only 33% for paddling. In addition to swimming mode, the transition to high performance propul- sion was associated with a shift from surface to submerged swimming providing a reduction in transport costs. The evolution of aquatic mam- mals from terrestrial ancestors required increased swimming performance with minimal compromise to terrestrial movement. Examination of mod- ern analogs to transitional swimming stages suggests that only slight mod- ification to the neuromotor pattern used for terrestrial locomotion is re- quired to allow for a change to lift-based propulsion.
The volume of air trapped in the feathers and the body density of 36 species of water bird were determined by water displacement experiments. Body density was higher and the volume of air trapped in plumage was lower in species that were most reliant on diving for foraging. Accordingly, we predict that habitually diving species have substantially reduced energy expenditure while underwater and correspondingly higher aerobic dive limits than infrequent divers. This agrees with field observations. Following Boyle's law, aerobic dive limits are predicted to increase with increasing dive depth due to a reduction in upthrust following volumetric reduction of feather-trapped air caused by hydrostatic pressure. It appears energetically more costly for diving birds to forage near the surface than at greater depths. Reduced plumage air to minimize underwater swimming costs, however, probably increases heat loss. The use of fat for insulation is not compatible with minimized flight costs. Frequent divers have higher flight costs than infrequent divers. We predict that the amount of air in the feathers and the amount of subcutaneous fat in aquatic birds are regulated in such a way as to minimize energy expenditure as a function of the temperature of the environment as well as diving and flying rhythms.
Buoyancy is far more important to locomotor costs of shallow diving than is hydrodynamic drag. Working with canvasbacks Aythya valisineria, redheads A. americana and lesser scaup A. affinis, the authors investigated factors affecting buoyancy in models of locomotor energetics. In scaup, an increase in body lipid from 35 to 190 g (from 5.4 to 22.3% of body mass) increases the energy costs of descent more through the inertial effects of high mass and added mass of entrained water (82.8% of change) than through greater work against drag (12.0%) or buoyancy (5.2%). Costs of foraging at the bottom are 20% lower in the fatter birds because increased inertial resistance to the buoyant force is greater than the increase in buoyancy. Maximal changes in body lipid and associated hypertrophied muscle raise overall costs of diving to a depth of 2m by only 2%. Such effects can be offset by altering respiratory and plumage air volumes (+15mL for a 155-g lipid increase) or the relative amount of time spent at the bottom. Hence, diving energetics contrast with the energetics of flight, which are strongly affected by body mass changes. Reduced buoyancy from compression of air spaces with depth lowers costs of bottom foraging in scaup by 24% at 1.2m and 36% at 2m. Mass-specific plumage air volume decreases with increasing body mass, and body tissues are incompressible relative to air. Thus, buoyancy decreases faster with increasing pressure in smaller birds and they become negatively buoyant at shallower depths (c43m for oldsquaw Clangula hyemalis). Ducks such as eiders Somateria weighing >1200 g and diving <60m probably never become negatively buoyant. (See 92L/09163) -from Authors
Optimisation of energy by aquatic mammals requires adaptations that reduce drag, and improve thrust production and efficiency. Drag is minimised by streamlining the body and appendages. Highly derived aquatic mammals have body shapes close to the optimal hydrodynamic design for drag reduction. There is no conclusive evidence for specialised drag reduction mechanisms, although decreasing hair density is associated with reduced drag. Improvement in thrust production and efficiency is accomplished by changes in propulsive mode and appendage design. Semiaquatic mammals employ. drag-based propulsion using paddles, whereas fully aquatic mammals use lift-based propulsion with hydrofoils. Because paddling generates thrust through half the stroke cycle, propulsive efficiency is low and energetic cost is high compared with that for mammals using hydrofoils. Lift-based swimming is a rapid and high-powered propulsive mode. Oscillations of the hydrofoil generate thrust throughout the stroke cycle. For cetaceans and pinnipeds, propulsive efficiency is approximately 80%, and transport cost is below that of semiaquatic mammals. Behavioural adaptations help minimise energy expenditure by swimming mammals. Submerged swimming avoids increased drag from energy lost in formation of surface waves. Porpoising and wave riding, characteristic of dolphins, can reduce the transport costs, allowing for longer-duration swimming at high speeds.
We compared the nonbreeding-season foraging behavior of lactating California sea lions (Zalophus californianus californianus (Lesson, 1828)) at San Miguel Island, California, during El Nio conditions in 1993 and non-El Nio conditions in 1996. Lactating females were instrumented with satellite-linked timedepth recorders between January and March in 1993 (n = 6) and 1996 (n = 10) and data were collected through May in each year. Females foraged northwest of the colony, up to 367km from it and 230km from the California coast. Mean dive depths ranged from 19.5to 279.3m, but most females achieved dives deeper than 400m. Most females fed exclusively in the offshore habitat, traveled farther from the colony, spent more time traveling, made deeper and longer dives, and terminated lactation earlier during the 1993 El Nio. The results suggest that prey were concentrated in the offshore habitat and located farther from the colony and deeper in the water column during El Nio. Females did not change their foraging direction, foraging-trip duration, foraging effort, or prey species consumed.
The diet of juvenile and adult female California sea lions (Zalophus californianus (Lesson, 1828)) at San Miguel Island, California, was estimated and compared using fecal and stable isotope analyses to determine dietary differences by age. Fecal samples were collected during 20022006 and prey remains were identified. Stable carbon (¹³C) and stable nitrogen (¹⁵N) isotope values were determined from plasma and fur obtained from yearlings, 2- to 3-year-old juveniles, and adult females during 2005 and 2006. Juveniles ate more than 15 prey taxa, whereas adult females consumed more than 33 taxa. Relative importance of prey was determined using percent frequency of occurrence (%FO). Engraulis mordax Girard, 1854, Sardinops sagax (Jenyns, 1842), Merluccius productus (Ayres, 1855), genus Sebastes Cuvier, 1829, and Loligo opalescens Berry, 1911 were the most frequently occurring (%FO> 10%) prey in the feces of both juvenile and adult female sea lions, although their importance varied between age groups. Only yearlings had significantly different isotopic values than older conspecifics, indicating that older juveniles were feeding at a similar trophic level and in similar habitats as adult females. Whereas each method had biases, combining the two provided a better understanding of the diet of California sea lions and intraspecific differences.
Rorqual baleen whales lunge feed by engulfment of tons of prey-laden water in a large and expandable buccal pouch. According to prior interpretations, feeding rorquals are brought to a near-halt at the end of each lunge by drag forces primarily generated by the open mouth. Accelerating the body from a standstill is energetically costly and is purported to be the key factor determining oxygen consumption in lunge-feeding rorquals, explaining the shorter dive times than expected given their sizes. Here, we use multi-sensor archival tags (DTAGs) sampling at high rates in a fine-scale kinematic study of lunge feeding to examine the sequence of events within lunges and how energy may be expended and conserved in the process of prey capture. Analysis of 479 lunges from five humpback whales reveals that the whales accelerate as they acquire prey, opening their gape in synchrony with strong fluke strokes. The high forward speed (mean depth rate: 2.0±0.32 m s(-1)) during engulfment serves both to corral active prey and to expand the ventral margin of the buccal pouch and so maximize the engulfed water volume. Deceleration begins after mouth opening when the pouch nears full expansion and momentum starts to be transferred to the engulfed water. Lunge-feeding humpback whales time fluke strokes throughout the lunge to impart momentum to the engulfed water mass and so avoid a near or complete stop, but instead continue to glide at ~1-1.5 m s(-1) after the lunge has ended. Subsequent filtration and prey handling appear to take an average of 46 s and are performed in parallel with re-positioning for the next lunge.
Efficient locomotion between prey resources at depth and oxygen at the surface is crucial for breath-hold divers to maximize time spent in the foraging layer, and thereby net energy intake rates. The body density of divers, which changes with body condition, determines the apparent weight (buoyancy) of divers, which may affect round-trip cost-of-transport (COT) between the surface and depth. We evaluated alternative predictions from external-work and actuator-disc theory of how non-neutral buoyancy affects round-trip COT to depth, and the minimum COT speed for steady-state vertical transit. Not surprisingly, the models predict that one-way COT decreases (increases) when buoyancy aids (hinders) one-way transit. At extreme deviations from neutral buoyancy, gliding at terminal velocity is the minimum COT strategy in the direction aided by buoyancy. In the transit direction hindered by buoyancy, the external-work model predicted that minimum COT speeds would not change at greater deviations from neutral buoyancy, but minimum COT speeds were predicted to increase under the actuator disc model. As previously documented for grey seals, we found that vertical transit rates of 36 elephant seals increased in both directions as body density deviated from neutral buoyancy, indicating that actuator disc theory may more closely predict the power requirements of divers affected by gravity than an external work model. For both models, minor deviations from neutral buoyancy did not affect minimum COT speed or round-trip COT itself. However, at body-density extremes, both models predict that savings in the aided direction do not fully offset the increased COT imposed by the greater thrusting required in the hindered direction.
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.
This book is not a conventional review of diving physiology. The coverage of the literature has been selective rather than en compassing, the emphasis has been on field studies rather than laboratory investigations, and the dive responses described are often discussed from the perspective of some of the flaws or weaknesses in the conclusions. Some of these points are of more historical interest to note how our concepts have evolved as we learn more about behavior and responses to natural diving in contrast to forced submersions in the laboratory. As a result there is a degree of evaluation of some experiments on my part that may seem obvious or controversial to the specialist. I have followed this planat times in order to aid the reader, who I hope is often an untergraduate or graduate stu dent, the nonspecialist, and the layman, in appreciating to some degree the level of dissatisfaction or skepticism about certain areas of research in diving physiology. In view of historical boundaries in vertebrate biology, the subject is of broad enough importance to catch the interest of a wide audience of readers if I have done my job well. For ex ample, of the major epochal transitions or events there have been in vertebrate history, three come immediately to mind: (1) The transition from aquatic to aerial respiration which ultimately led to a broad occupation of terrestrial habitats. (2) The development of endothermy.
There was an error published in J. Exp. Biol. 219, 2458-2468. Eqn 1 was presented incorrectly. A '-1' was missing after the ratio of densities, and the subscript of the first instance of the density of seawater (Psw) was given incorrectly as 'w' instead of 'sw'. The original equation was: (Formula presented) The correct equation is as follows (Formula presented) This error was corrected on 21 September 2016 in the full-text and PDF versions of this article. The Advance Article and print version of the article remain unchanged. The authors apologise to the readers for any inconvenience this may have caused.
Pulmonary shunts in seals and sea lions were determined before and during dives to simulated depths up to 100 m. Five young harbor seals weighing 36-50 kg and two young sea lions weighing 21-40 kg were dived in a compression chamber. Before and during the dives, blood samples were obtained from the aorta and usually the pulmonary artery. Arterial O₂, and CO₂ tensions, hemoglobin concentration, and venous O₂ contents were determined. From these data the physiological pulmonary shunt of the lung could be calculated. These shunts ranged from 8.4% at the surface to a pulmonary shunt due to compression of over 70% during a dive to 100 m. As discussed, structure of the terminal airways might be expected to affect the rate that alveoli would compress and develop shunts. However, we conclude that at pressures of less than 8 atm (equivalent to 70-m depth) there is not a marked difference in the degree of compression shunt between sea lions and harbor seals even though there are striking differences in terminal airway anatomy.
During the 1983 El Niño event, California sea lions (Zalophus californianus) and Galapagos fur seals (Arctocephalus galapagoensis) responded to the reduction in food availability by extending their foraging trips to sea and delivering less milk to their pups (Trillmich and Limberger 1985; Ono et al. 1987). These observed changes likely reflected a change in foraging tactics as animals attempted to compensate for a reduced food supply. The manner in which these foraging patterns were altered, however, still remains unclear.
1. The measurement of energy expenditures in free-ranging animals is essential if we are to understand fully the interaction between a species and its environment. This study examined the validity of heart rate (fH) and doubly labelled water (DLW) as measures of field metabolic rate (FMR) in California Sea Lions (Zalophus californianus). 2. Oxygen consumption and CO2 production were measured over 24 h by direct respirometry in six juvenile sea lions. The respirometer consisted of a hood over a flume in which the sea lions were exercised to various levels for 15 min periods throughout each experiment. The exercise regime produced a mean metabolic rate which was 2.3 times the predicted basal metabolic rate (BMR) with mean maxima of 6.27 times the predicted BMR. 3. Simultaneously with direct respirometry, mean CO2 production was estimated using DLW and O2 consumption was estimated using fH, which had previously been calibrated against O2 consumption. 4. The mean\pmSD O2 consumptions from direct respirometry, fH and DLW were 11.80\pm2.40, 11.95\pm2.17 and 15.01\pm3.77 ml min-1 kg-1 respectively. Paired Student's t-tests showed no significant difference between O2 consumption by direct respirometry and the estimates from DLW and fH. DLW measurements ranged from -10% to +86% of the direct respirometry measurements (mean +36.4%) and fH measurements ranged from -28% to +23% of the direct respirometry measurements (mean +2.7%). 5. The range of estimated metabolic rates from fH was largely owing to individual differences in the slopes of the linear relationship between fH and O2 consumption. The range of metabolic rates from DLW could be partly attributed to the short duration of the experiments (24-25 h) but this was shown not to be the cause of the tendency to overestimate metabolic rate from DLW. It was concluded that both DLW and fH are valid methods for measuring FMR in California Sea Lions although it is possible that FMR could be overestimated when using DLW.
We present a theoretical model for calculating the locomotion cost of
breath-hold divers. Starting from basic principles of mechanics, we calculate
the work that the diver has to provide with propulsion for counterbalance the
action of the drag, the buoyant force and the weight during the immersion. The
basal metabolic rate and the efficiency to transform chemical energy in
propulsion are also considered for the calculation of the total energy cost of
a dive. The dependency on the diver and dive characteristics and possible
optimisations are analysed and discussed. Our results are compared to
observation on different breath-hold diving animals. The model confirms the
good adaptation of dolphin for deep dives, and it gives some insights for a
possible explanation of the exhalation of air before diving observed in seals.
A comparison between predicted and observed swim velocities of different
breath-hold mammals confirms the importance of the role of the diving reflex.
The anatomy and volume of the penguin respiratory system contribute significantly to pulmonary baroprotection, the body O2 store, buoyancy and hence the overall diving physiology of penguins. Therefore, three-dimensional reconstructions from computerized tomographic (CT) scans of live penguins were utilized to measure lung volumes, air sac volumes, tracheobronchial volumes and total body volumes at different inflation pressures in three species with different dive capacities [Adélie (Pygoscelis adeliae), king (Aptenodytes patagonicus) and emperor (A. forsteri) penguins]. Lung volumes scaled to body mass according to published avian allometrics. Air sac volumes at 30 cm H2O (2.94 kPa) inflation pressure, the assumed maximum volume possible prior to deep dives, were two to three times allometric air sac predictions and also two to three times previously determined end-of-dive total air volumes. Although it is unknown whether penguins inhale to such high volumes prior to dives, these values were supported by (a) body density/buoyancy calculations, (b) prior air volume measurements in free-diving ducks and (c) previous suggestions that penguins may exhale air prior to the final portions of deep dives. Based upon air capillary volumes, parabronchial volumes and tracheobronchial volumes estimated from the measured lung/airway volumes and the only available morphometry study of a penguin lung, the presumed maximum air sac volumes resulted in air sac volume to air capillary/parabronchial/tracheobronchial volume ratios that were not large enough to prevent barotrauma to the non-collapsing, rigid air capillaries during the deepest dives of all three species, and during many routine dives of king and emperor penguins. We conclude that volume reduction of airways and lung air spaces, via compression, constriction or blood engorgement, must occur to provide pulmonary baroprotection at depth. It is also possible that relative air capillary and parabronchial volumes are smaller in these deeper-diving species than in the spheniscid penguin of the morphometry study. If penguins do inhale to this maximum air sac volume prior to their deepest dives, the magnitude and distribution of the body O2 store would change considerably. In emperor penguins, total body O2 would increase by 75%, and the respiratory fraction would increase from 33% to 61%. We emphasize that the maximum pre-dive respiratory air volume is still unknown in penguins. However, even lesser increases in air sac volume prior to a dive would still significantly increase the O2 store. More refined evaluations of the respiratory O2 store and baroprotective mechanisms in penguins await further investigation of species-specific lung morphometry, start-of-dive air volumes and body buoyancy, and the possibility of air exhalation during dives.
© 2015. Published by The Company of Biologists Ltd.
A full derivation is presented for the vortex theory of hovering flight outlined in preliminary reports. The theory relates the lift produced by flapping wings to the induced velocity and power of the wake. Suitable forms of the momentum theory are combined with the vortex approach to reduce the mathematical complexity as much as possible. Vorticity is continuously shed from the wings in sympathy with changes in wing circulation. The vortex sheet shed during a half-stroke convects downwards with the induced velocity field, and should be approximately planar at the end of a half-stroke. Vorticity within the sheet will roll up into complicated vortex rings, but the rate of this process is unknown. The exact state of the sheet is not crucial to the theory, however, since the impulse and energy of the vortex sheet do not change as it rolls up, and the theory is derived on the assumption that the extent of roll-up is negligible. The force impulse required to generate the sheet is derived from the vorticity of the sheet, and the mean wing lift is equal to that impulse divided by the period of generation. This method of calculating the mean lift is suitable for unsteady aerodynamic lift mechanisms as well as the quasi-steady mechanism. The relation between the mean lift and the impulse of the resulting vortex sheet is used to develop a conceptual artifice - a pulsed actuator disc - that approximates closely the net effect of the complicated lift forces produced in hovering. T he disc periodically applies a pressure impulse over some defined area, and is a generalized form of the Froude actuator disc from propeller theory. The pulsed disc provides a convenient link between circulatory lift and the powerful momentum and vortex analyses of the wake. The induced velocity and power of the wake are derived in stages, starting with the simple Rankine-Froude theory for the wake produced by a Froude disc applying a uniform, continuous pressure to the air. The wake model is then improved by considering a ‘modified’ Froude disc exerting a continuous, but non-uniform pressure. This step provides a spatial correction factor for the Rankine-Froude theory, by taking into account variations in pressure and circulation over the disc area. Finally, the wake produced by a pulsed Froude disc is analysed, and a temporal correction factor is derived for the periodic application of spatially uniform pressures. Both correction factors are generally small, and can be treated as independent perturbations of the Rankine-Froude model. Thus the corrections can be added linearly to obtain the total correction for the general case of a pulsed actuator disc with spatial and temporal pressure variations. The theory is compared with Rayner’s vortex theory for hovering flight. Under identical test conditions, numerical results from the two theories agree to within 3%. Rayner presented approximations from his results to be used when applying his theory to hovering animals. These approximations are not consistent with my theory or with classical propeller theory, and reasons for the discrepancy are suggested.
Expressions have been derived for an estimate of the average coefficient of lift, for the variation in bending moment or torque caused by wind forces and by inertia forces, and for the power output during hovering flight on one spot when the wings move according to a horizontal figure-of-eight. In both hummingbirds and Drosophila the flight is consistent with steady-state aerodynamics, the average lift coefficient being 1·8 in the hummingbird and o-8 in Drosophila. The aerodynamic or hydraulic efficiency is 0·5 in the hummingbird and 0·3 in Drosophila, and in both types the aerodynamic power output is 22–24 cal/g body weight/h. The total mechanical power output is 39 cal g−1 h−1 in the hummingbird because of the extra energy needed to accelerate the wing-mass. It is 24 cal g−1 h−1 in Drosophila in which the inertia term is negligible because the wing-stroke frequency is reduced to the lowest possible value for sustained flight. In both animals the mechanical efficiency of the flight muscles is 0·2. It is argued that the tilt of the stroke plane relative to the horizontal is an adaptation to the geometrically unfavourable induced wind and to the relatively large lift/drag ratio seen in many insects. The vertical movements at the extreme ends may serve to reduce the interaction between the shed ‘stopping’ vortex and the new bound vortex of opposite sense which has to be built up during the early part of the return stroke. Two additional non-steady flow situations may exist at either end of the stroke, delayed stall and delayed build-up of circulation (Wagner effect), but since they have opposite effects it is probable that the resultant force is of about the same magnitude as that estimated for a steady-state situation. Most insects have an effective elastic system to counteract the adverse effect of wing-inertia, but small fast-moving vertebrates have not. It is argued that the only material available for this purpose in this group is elastin and that it is unsuited at the rates of deformation required because recent measurements have shown that the damping is relatively high, probably due to molecular factors.
The elongated-body theory of the reactive forces on a fish moving in
water (that is, forces resulting from the inertia of associated water
movements) is extended so that a prediction of instantaneous reactive
force between fish and water is obtained for fish motions of arbitrary
amplitude, regular or irregular (secion 2). A preliminary application of
the theory to the balance of reactive thrust and resistive drag in
regular carangiform swimming of fishes with slender caudal fins is made
(section 3). Comparison with data (Bainbridge 1963) on the dace
Leuciscus suggests that an important feature of this balance may be a
substantial enhancement of drag for such fishes when swimming movements
commence, an enhancement here interpreted in terms of a
boundary-layer-thinning mechanism first suggested by Dr Quentin Bone.
The diving patterns of 10 adult female California sea lions (Zalophus californianus) were examined during the summer breeding season on San Miguel Island, California, in 1982 and 1983 using time–depth recorders. During 17 feeding trips, representing 40.6 days at sea, animals made over 8900 dives, the deepest of which was estimated at 274 m, while the longest was 9.9 min. The majority of dives, however, were less than 3 min in duration and 80 m in depth. From estimates of body oxygen stores, we predict that dives up to 5.8 min can be supported aerobically. Therefore, cost–benefit considerations based on prey availability and encounter rate may be more important than physiological limits in shaping the foraging patterns of Zalophus. Sea lions were active virtually throughout their time at sea, resting on the surface for only 3% of the average trip. Peak diving frequency occurred during the twilight hours near sunrise and sunset. Dives were frequent, however, during all hours of the day and were typically clustered into bouts that lasted a mean (±SD) of 3.3 ± 1.5 h. We suggest that these bouts represent active feeding on discrete prey patches. During short bouts (<3 h), dive depth was less variable than for dives occurring between bouts. During longer bouts, dive depth changed in a manner consistent with pursuit of vertically migrating prey. During the 1983 El Niño, sea lions compensated for a reduction in food availability by lengthening dive bouts. These seasonal and diel variations in diving patterns suggest that the rate of prey encounter strongly influences the depth and duration of individual dives.
Although the cheetah is recognised as the fastest land animal, little is known about other aspects of its notable athleticism, particularly when hunting in the wild. Here we describe and use a new tracking collar of our own design, containing a combination of Global Positioning System (GPS) and inertial measurement units, to capture the locomotor dynamics and outcome of 367 predominantly hunting runs of five wild cheetahs in Botswana. A remarkable top speed of 25.9 m s(-1) (58 m.p.h. or 93 km h(-1)) was recorded, but most cheetah hunts involved only moderate speeds. We recorded some of the highest measured values for lateral and forward acceleration, deceleration and body-mass-specific power for any terrestrial mammal. To our knowledge, this is the first detailed locomotor information on the hunting dynamics of a large cursorial predator in its natural habitat.
California sea lion (Zulophus calijoyniunus) scat and spewing samples collected at three rookeries in south- ern California during 1981-95 were used to determine how sea lions utilized the market squid (Lol&o opalescens) resource. The samples revealed that market squid is one of the most important prey of sea lions in southern California, occurring in 35% to 44% of scat samples from San Nicolas Island (SNI), San Clemente Island (SCI), and Santa Barbara Island (SBI). It is eaten by sea lions throughout the year, but most often during fall and win- ter, and patterns suggest periods of high and low con- sumption associated with prevailing oceanographic conditions and, possibly, with squid abundance and movements. Percent frequency of occurrence values for market squid in scat samples collected seasonally from SNI were positively correlated with those from SCI (Y = 0.78), and samples collected during summer at SBI were positively correlated with summer samples from SCI (Y = 0.82) and SNI (Y = 0.85). Landings of market squid at ports in southern California and percent oc- currence values of market squid in scat samples collected seasonally were positively correlated for SNI (Y = 0.66) and SCI (Y = 0.74), but not for summer samples from SBI (Y = 0.25). Sea lions eat squid with dorsal mantle lengths from 10 to 235 mm (mean = 127 mm). Signif- icant seasonal, annual, and interisland differences (P < 0.001) were found in the size of squid consumed by sea lions. Significant differences (P < 0.001) were found in size of squid between scats and spewing, and between individual samples.
Carnivora includes three independent evolutionary transitions to the marine environment: pinnipeds (seals, sea lions, and walruses), sea otters, and polar bears. Among these, only the pinnipeds have retained two forms of insulation, an external fur layer and an internal blubber layer for keeping warm in water. In this study we investigated key factors associated with the transition to the use of blubber, by comparing blubber characteristics among the pinnipeds. Characteristics included gross morphology (blubber thickness), fat composition (fatty acid profiles, percentage lipid, and water), and thermal conductivity. Sea lions, phocids, and walrus, which have lower fur densities than fur seals, have thicker blubber layers than fur seals (P < 0.001). Comparisons of lipid content, water content, and fatty acid composition indicated significant differences in the composition of the inner and outer regions of the blubber between groups (P < 0.001), consistent with the hypothesis that phocids and sea lions utilize the outer layer of their blubber primarily for thermal insulation, and the inner layer for energy storage. Fur seals, by contrast, rely more on their fur for thermal insulation, and utilize their blubber layer primarily for energy storage. Comparing across carnivore species, differences in total insulation (fur and/or blubber) are influenced substantially by body size and habitat, and to a lesser extent by latitudinal climate. Overall, these results indicate consistent evolutionary trends in the transition to blubber and evidence for convergent evolution of thermal traits across lineages.