Early diving behaviour in juvenile penguins: improvement or selection processes

The early life stage of long-lived species is critical to the viability of population, but is poorly understood. Longitudinal studies are needed to test whether juveniles are less efficient foragers than adults as has been hypothesized. We measured changes in the diving behaviour of 17 one-year-old king penguins Aptenodytes patagonicus at Crozet Islands (subantartic archipelago) during their first months at sea, using miniaturized tags that transmitted diving activity in real time. We also equipped five non-breeder adults with the same tags for comparison. The data on foraging performance revealed two groups of juveniles. The first group made shallower and shorter dives that may be indicative of early mortality while the second group progressively increased their diving depths and durations, and survived the first months at sea. This surviving group of juveniles required the same recovery durations as adults, but typically performed shallower and shorter dives. There is thereby a relationship between improved diving behaviour and survival in young penguins. This long period of improving diving performance in the juvenile life stage is potentially a critical period for the survival of deep avian divers and may have implications for their ability to adapt to environmental change.     

Running, swimming and diving modifies neuroprotecting globins in the mammalian brain

The vulnerability of the human brain to injury following just a few minutes of oxygen deprivation with submergence contrasts markedly with diving mammals, such as Weddell seals (Leptonychotes weddellii), which can remain underwater for more than 90 min while exhibiting no neurological or behavioural impairment. This response occurs despite exposure to blood oxygen levels concomitant with human unconsciousness. To determine whether such aquatic lifestyles result in unique adaptations for avoiding ischaemic-hypoxic neural damage, we measured the presence of circulating (haemoglobin) and resident (neuroglobin and cytoglobin) oxygen-carrying globins in the cerebral cortex of 16 mammalian species considered terrestrial, swimming or diving specialists. Here we report a striking difference in globin levels depending on activity lifestyle. A nearly 9.5-fold range in haemoglobin concentration (0.17-1.62 g Hb 100 g brain wet wt(-1)) occurred between terrestrial and deep-diving mammals; a threefold range in resident globins was evident between terrestrial and swimming specialists. Together, these two globin groups provide complementary mechanisms for facilitating oxygen transfer into neural tissues and the potential for protection against reactive oxygen and nitrogen groups. This enables marine mammals to maintain sensory and locomotor neural functions during prolonged submergence, and suggests new avenues for averting oxygen-mediated neural injury in the mammalian brain.     

A thorough and quantified method for classifying seabird diving behaviour

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

Locomotion in diving elephant seals: physical and physiological constraints

To better understand how elephant seals (Mirounga angustirostris) use negative buoyancy to reduce energy metabolism and prolong dive duration, we modelled the energetic cost of transit and deep foraging dives in an elephant seal. A numerical integration technique was used to model the effects of swim speed, descent and ascent angles, and modes of locomotion (i.e. stroking and gliding) on diving metabolic rate, aerobic dive limit, vertical displacement (maximum dive depth) and horizontal displacement (maximum horizontal distance along a straight line between the beginning and end locations of the dive) for aerobic transit and foraging dives. Realistic values of the various parameters were taken from previous experimental data. Our results indicate that there is little energetic advantage to transit dives with gliding descent compared with horizontal swimming beneath the surface. Other factors such as feeding and predator avoidance may favour diving to depth during migration. Gliding descent showed variable energy savings for foraging dives. Deep mid-water foraging dives showed the greatest energy savings (approx. 18%) as a result of gliding during descent. In contrast, flat-bottom foraging dives with horizontal swimming at a depth of 400m showed less of an energetic advantage with gliding descent, primarily because more of the dive involved stroking. Additional data are needed before the advantages of gliding descent can be fully understood for male and female elephant seals of different age and body composition. This type of data will require animal-borne instruments that can record the behaviour, three-dimensional movements and locomotory performance of free-ranging animals at depth.     

The winter distribution of chinstrap penguins from two breeding sites in the South Shetland Islands of Antarctica

Satellite telemetry was used to determine the winter movements of eight chinstrap penguins from two breeding colonies in the South Shetland Islands, Antarctica during the 2000 and 2004 austral winters. Chinstrap penguins foraged largely inshore, on the shelf, north of the South Shetland Islands during 2000, but foraged mainly offshore in pelagic waters in 2004. Analyses of foraging trip durations during the chick-rearing periods that preceded the 2000 and 2004 winters suggest that prey were more abundant inshore during the summer of 2000 than in 2004. Oceanographic data further revealed the presence of a strong shelf-slope front in 2000 that was absent in 2004. In addition, two of the six chinstrap penguins from the colony in Admiralty Bay migrated from the South Shetland Islands region to the vicinity of the South Orkney and South Sandwich Islands, distances of 800 and 1,300 km, respectively. We postulate that the differences in winter migratory behavior among chinstrap penguins from this colony may reflect individual ties to different ancestral epicenters of chinstrap populations; one older and local in the South Shetland Islands and one relatively recent, arising from the emigration of chinstrap penguins that occurred during the expansion of this species in the mid-1900s.     

Seasonal changes in fast-starts in the short-horn sculpin: integration of swimming behaviour and muscle performance

In short-horn sculpin Myoxocephalus scorpius , the power requirements for fast-start swimming and the length-specific velocity of the curvature wave travelling down the spine ( Û ) were not influenced significantly by acclimation to summer and winter conditions at test temperatures of 5 and 15° C. However, in-vivo and in-vitro muscle performance exhibited acclimation responses at 15° C. Seasonal acclimation altered the escape performance curves for power and Û significantly over a wider temperature range of 0·8–20° C. Û was significantly higher at 20° C in the summer- than winter-acclimation group. The acclimation of lower levels of physiological organization at 15° C may thus serve to extend the thermal limits for escape performance in summer acclimated fish.     

The tracheal supply and muscle metabolism during muscle growth in the puparium of Calliphora vomitoria

Thirty hours after puparium formation in Calliphora, the larval tracheal system is replaced by an air-filled pupal system. This is characterized initially by many tufts of tracheae and coiled tracheoles lying in the blood. Between the third and fourth day, the sixth dorsal longitudinal flight muscles are practically without attached tracheae and their longitudinal growth can partially occur when oxygen uptake is inhibited with potassium cyanide. Sodium iodoacetate prevents muscle growth. After the fifth day of development the pupal tracheoles spread out over the surface of the developing adult muscles. Between the seventh and ninth day, longitudinal growth and increases in the diameter of the myofibrils are halted by cyanide and iodoacetate. Some longitudinal growth and an increase in the total protein content of the muscles can occur in 1% oxygen. Air filling of the adult tracheae takes place 2–3 hr before the emergence of the adult and is accompanied by an increase in oxygen consumption of the thorax. The metabolism and growth of the muscles is discussed with respect to their changing oxygen supply.     

Krill-feeding behaviour of gentoo penguins as shown by animal-borne camera loggers

Animal-borne camera loggers were used to examine the patterns of prey encounter and feeding behaviour of gentoo penguins at King George Island, Antarctica. The still images from the camera loggers showed that the penguins encountered the swarms of krill for 25.5% (range: 8–38%) of their dives (>5 m) on average, during their foraging trips (mean duration of 5.4 h, n = 7 trips). They encountered krill swarms during the dives to 10–70 m depth, in pelagic as well as benthic habitats. In the benthic habitat, the penguins swam just above the sea floor and headed downward over a krill swarm, probably using the sea floor to assist them to feed on mobile swarms. The shallow coastal waters would be the important foraging habitat of gentoo penguins breeding in King George Island.     

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

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

Thermal substitution and aerobic efficiency: measuring and predicting effects of heat balance on endotherm diving energetics

For diving endotherms, modelling costs of locomotion as a function of prey dispersion requires estimates of the costs of diving to different depths. One approach is to estimate the physical costs of locomotion (Pmech) with biomechanical models and to convert those estimates to chemical energy needs by an aerobic efficiency (eta=Pmech/Vo2) based on oxygen consumption (Vo2) in captive animals. Variations in eta with temperature depend partly on thermal substitution, whereby heat from the inefficiency of exercising muscles or the heat increment of feeding (HIF) can substitute for thermogenesis. However, measurements of substitution have ranged from lack of detection to nearly complete use of exercise heat or HIF. This inconsistency may reflect (i) problems in methods of calculating substitution, (ii) confounding mechanisms of thermoregulatory control, or (iii) varying conditions that affect heat balance and allow substitution to be expressed. At present, understanding of how heat generation is regulated, and how heat is transported among tissues during exercise, digestion, thermal challenge and breath holding, is inadequate for predicting substitution and aerobic efficiencies without direct measurements for conditions of interest. Confirming that work rates during exercise are generally conserved, and identifying temperatures at those work rates below which shivering begins, may allow better prediction of aerobic efficiencies for ecological models.     

Metal concentrations in the liver and kidney of aquatic mammals and penguins

We determined the hepatic and renal concentrations of Cd, Pb, Zn, Cu, and Fe in (1) marine mammals (three bottle-nosed dolphins, six California sea lions, and one sea otter), (2) freshwater and brackish-water mammals (one Oriental short-clawed otter and four European river otters), and (3) sea birds (three rock-hopper penguins, two king penguins, three Humboldt penguins, four Macaroni penguins, and four Magellanic penguins), all of which were kept in a zoo and an aquarium in Japan. We investigated the species-specificity of Cd accumulation in these aquatic animals. We also presented the basic data on metal concentrations. The concentrations of Cd in liver and kidney tended to be higher in marine mammals than in freshwater mammals. Many penguins, sea birds, showed high Cd concentrations. These results suggest that the habits of these animal species may be involved in accumulation of Cd. Pb concentrations were below the detection limit or low in both liver and kidney [not detected (ND)=0.132 μg/g and ND=0.183 μg/g, respectively]. The hepatic concentrations of Zn and Cu were high in young animals. In penguins, a positive correlation was found between the Zn and Cd concentrations in the liver and kidney and between the Cu and Cd concentrations in the liver. Individual variation was large in Fe concentration (48–3746 μg/g in the liver and 51–980 μg/g in the kidney).     

A review of fish swimming mechanics and behaviour in altered flows

Fishes suspended in water are subject to the complex nature of three-dimensional flows. Often, these flows are the result of abiotic and biotic sources that alter otherwise uniform flows, which then have the potential to perturb the swimming motions of fishes. The goal of this review is to highlight key studies that have contributed to a mechanistic and behavioural understanding of how perturbing flows affect fish. Most of our understanding of fish behaviour in turbulence comes from observations of natural conditions in the field and laboratory studies employing controlled perturbations, such as vortices generated in the wake behind simple geometric objects. Laboratory studies have employed motion analysis, flow visualization, electromyography, respirometry and sensory deprecation techniques to evaluate the mechanisms and physiological costs of swimming in altered flows. Studies show that flows which display chaotic and wide fluctuations in velocity can repel fishes, while flows that have a component of predictability can attract fishes. The ability to maintain stability in three-dimensional flows, either actively with powered movements or passively using the posture and intrinsic compliance of the body and fins, plays a large role in whether fish seek out or avoid turbulence. Fish in schools or current-swept habitats can benefit from altered flows using two distinct though not mutually exclusive mechanisms: flow refuging (exploiting regions of reduced flow relative to the earth frame of reference) and vortex capture (harnessing the energy of environmental vortices). Integrating how the physical environment affects organismal biomechanics with the more complex issue of behavioural choice requires consideration beyond simple body motions or metabolic costs. A fundamental link between these two ways of thinking about animal behaviour is how organisms sense and process information from the environment, which determines when locomotor behaviour is initiated and modulated. New data are presented here which show that behaviour changes in altered flows when either the lateral line or vision is blocked, showing that fish rely on multi-modal sensory inputs to negotiate complex flow environments. Integrating biomechanics and sensory biology to understand how fish swim in turbulent flow at the organismal level is necessary to better address population-level questions in the fields of fisheries management and ecology.     

Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean

1. Climatic variation outside the breeding season affects fluctuations in population numbers of seabirds and marine mammals. A challenge in identifying the underlying biological mechanisms is the lack of information on their foraging strategies during winter, when individuals migrate far from their breeding grounds. 2. We investigated the temporal variability in resource partitioning within the guild of five sympatric Subantarctic penguins and fur seals from Crozet Islands. The stable isotopic ratios of carbon (delta(13)C) and nitrogen (delta(15)N) for whole blood were measured for penguins and fur seals, as were the isotopic ratios for penguin nails and food. Animals were sampled at two periods, during breeding in summer and at their arrival in the colonies in spring (hereafter winter, since the temporal integration of blood amounting to several months). 3. In summer, delta(13)C and delta(15)N for blood samples defined three foraging areas and two trophic levels, respectively, characterizing four nonoverlapping trophic niches. King penguins and female Antarctic and Subantarctic fur seals are myctophid eaters foraging in distinct water masses, while both macaroni and rockhopper penguins had identical isotopic signatures indicating feeding on crustaceans near the archipelago. 4. Isotopic ratios were almost identical in summer and winter suggesting no major changes in the species niches, and hence, in the trophic structure of the guild during the nonbreeding period. A seasonal difference, however, was the larger variances in delta(13)C (and also to a lesser extent in delta(15)N) values in winter, thus verifying our hypothesis that trophic niches widen when individuals are no longer central place foragers. 5. Winter isotopic ratios of macaroni penguins and male Antarctic fur seals had large variances, indicating individual foraging specializations. The range of delta(13)C and delta(15)N values of male fur seals showed, respectively, that they dispersed over a wide latitudinal gradient (from Antarctica to north of the archipelago) and fed on different prey (crustaceans and fish). 6. By comparing summer and winter isotopic ratios and examining the summer diet, we highlight the feeding habits of marine predators that were not previously addressed. The findings have a number of implications for understanding the functioning of the pelagic ecosystem and on the demography of these species.     

Skeletal muscle histology and biochemistry of an elite sprinter, the African cheetah

To establish a skeletal muscle profile for elite sprinters, we obtained muscle biopsy samples from the vastus lateralis, gastrocnemius and soleus of African cheetahs (Acinonyx jubatus). Muscle ultrastructure was characterized by the fiber type composition and mitochondrial volume density of each sample. Maximum enzyme activity, myoglobin content and mixed fiber metabolite content were used to assess the major biochemical pathways. The results demonstrate a preponderance of fast-twitch fibers in the locomotor muscles of cheetahs; 83% of the total number of fibers examined in the vastus lateralis and nearly 61% of the gastrocnemius were comprised of fast-twitch fibers. The total mitochondrial volume density of the limb muscles ranged from 2.0 to 3.9% for two wild cheetahs. Enzyme activities reflected the sprinting capability of the cheetah. Maximum activities for pyruvate kinase and lactate dehydrogenase in the vastus lateralis were 1519.00 ± 203.60 and 1929.25±482.35 μmol min⁻¹ · g wet wt⁻¹, respectively, and indicated a high capacity for glycolysis. This study demonstrates that the locomotor muscles of cheetahs are poised for anaerobically based exercise. Fiber type composition, mitochondrial content and glycolytic enzyme capacities in the locomotor muscles of these sprinting cats are at the extreme range of values for other sprinters bred or trained for this activity including greyhounds, thoroughbred horses and elite human athletes. Accepted: 5 June 1997     

The optimal allocation of time and respiratory metabolism over the dive cycle

Because anaerobic metabolism is much less efficient than aerobicmetabolism in supplying energy, it is widely believed that diversrely predominantly on aerobic metabolism for diving. In thispaper, a time budget model, which assumes that the diver canuse either completely aerobic or partially aerobic metabolismwith additional anaerobic metabolism for diving, is developedand is used to make predictions about patterns in optimal allocationof time and respiratory metabolism during the dive cycle. Theresults derived from the model are (1) a diver that can varythe ratio of energy supplied anaerobically to total energy spentduring dive time is favored by natural selection, but the patternsof time allocation over the dive cycle by the diver do not differ fromthose of a diver that cannot vary the ratio. (2) Even if itis assumed that divers switch their metabolism for diving, anobvious upturn in the surface time with respect to dive timedoes not occur at the aerobic dive limit (ADL) but occurs beyondthe ADL. (3) Use of additional anaerobic metabolism can be favoredfor dives shorter than the ADL. These findings provide a usefulguide to understanding the factors that limit diving behavior.     

Genome analysis and signature discovery for diving and sensory properties of the endangered Chinese alligator

Crocodilians are diving reptiles that can hold their breath under water for long periods of time and are crepuscular animals with excellent sensory abilities. They comprise a sister lineage of birds and have no sex chromosome. Here we report the genome sequence of the endangered Chinese alligator (Alligator sinensis) and describe its unique features. The next-generation sequencing generated 314 Gb of raw sequence, yielding a genome size of 2.3 Gb. A total of 22 200 genes were predicted in Alligator sinensis using a de novo, homology- and RNA-based combined model. The genetic basis of long-diving behavior includes duplication of the bicarbonate-binding hemoglobin gene, co-functioning of routine phosphate-binding and special bicarbonate-binding oxygen transport, and positively selected energy metabolism, ammonium bicarbonate excretion and cardiac muscle contraction. Further, we elucidated the robust Alligator sinensis sensory system, including a significantly expanded olfactory receptor repertoire, rapidly evolving nerve-related cellular components and visual perception, and positive selection of the night vision-related opsin and sound detection-associated otopetrin. We also discovered a well-developed immune system with a considerable number of lineage-specific antigen-presentation genes for adaptive immunity as well as expansion of the tripartite motif-containing C-type lectin and butyrophilin genes for innate immunity and expression of antibacterial peptides. Multifluorescence in situ hybridization showed that alligator chromosome 3, which encodes DMRT1, exhibits significant synteny with chicken chromosome Z. Finally, population history analysis indicated population admixture 0.60-1.05 million years ago, when the Qinghai-Tibetan Plateau was uplifted.     

Leg-attached data loggers do not modify the diving performances of a foot-propelled seabird

Global location sensors (GLS) are increasingly being used to determine animal position at sea. Their small size and weight means that they can be attached to the leg of volant birds with supposedly little impact on the flight ability. However, very few studies have investigated the impact that foot-attached devices may have on the diving ability of foot-propelled seabirds. We compared the diving activity of two groups of free-ranging great cormorants Phalacrocorax carbo carbo , both groups carrying identical time-depth recorders attached to the tail, and one group also having leg-attached GLS. Our results showed that there were no differences between the two groups in any of the diving parameters investigated, at least over the short term. Caution should be exercised when extrapolating to other species, especially those smaller than great cormorants, and also when deploying GLS over longer periods.     

The muscle twitch and the maximum swimming speed of giant bluefin tuna, Thunnus thynnus L.

Sustained swimming of bluefin tuna was analysed from video recordings made of a captive patrolling fish school [lengths (L) 1.7–3.3 m, body mass (M) 54–433 kg]. Speeds ranged from 0.6 to 1.2 L s⁻¹ (86–260 km day⁻¹) while stride length during steady speed swimming varied between 0.54 and 0.93 L. Maximum swimming speed was estimated by measuring twitch contraction of the anaerobic swimming muscle in pithed fish 5 min after death. Muscle contraction time increased from the shortest just behind the head (30–50 ms at 20% L) to the longest at the tail peduncle (80–90 ms at 80% L) (all at 28°C). A fish (L = 2.26 m) with a muscle contraction time of 50 ms at 25% L can have a maximum tail beat frequency of 10 Hz and maximum swimming speed of 15m s⁻¹ (54km h⁻¹) with a stride length of 0.65L. With a stride length of 1 L a speed of 22.6 m s⁻¹ (81.4 km h⁻¹) is possible. Power used at maximum speed was estimated for this fish at between 10 and 40 kW, with corresponding values for the drag coefficient at a Reynolds number of 4.43 × 10⁷ of 0.0007 and 0.0027.