The early life of king penguins: ontogeny of dive capacity and foraging behaviour in an expert diver.

The period of emancipation in seabirds, when juveniles change from a terrestrial existence to a life at sea, is associated with many challenges. Apart from finding favourable foraging sites, they have to develop effective prey search patterns and physiological capacities that enable them to capture sufficient prey to meet their energetic needs. Animals that dive to forage, such as king penguins (Aptenodytes patagonicus), need to acquire an adequate breath-hold capacity, allowing them to locate and capture prey at depth. To investigate the ontogeny of their dive capacity and foraging performance, we implanted juvenile king penguins before their first departure to sea and also adult breeders with a data-logger recording pressure and temperature. We found that juvenile king penguins possess a remarkable dive capacity when leaving their natal colony, enabling them to conduct dives in excess of 100 m within their first week at sea. Despite this, juvenile dive/foraging performance, investigated in relation to dive depth, remained below the adult level throughout their first year at sea, probably reflecting physiological limitations as a result of incomplete maturation. A significantly shallower foraging depth of juveniles, particularly during their first 5 months at sea, could also indicate differences in foraging strategy and targeted prey. The initially greater wiggle rate suggests that juveniles fed opportunistically and also targeted different prey from adults and/or that many of the wiggles of juveniles reflect unsuccessful prey-capture attempts, indicating a lower foraging proficiency. After 5 months, this difference disappeared, suggesting sufficient physical maturation and improvement of juvenile foraging skills.

The dive performance of immature king penguins following their annual molt suggests physiological constraints.

Like all birds, penguins undergo periodic molt, during which they replace old feathers. However, unlike other birds, penguins replace their entire plumage within a short period while fasting ashore. During molt, king penguins (Aptenodytes patagonicus) lose half of their initial body mass, most importantly their insulating subcutaneous fat and half of their pectoral muscle mass. The latter might challenge their capacity to generate and sustain a sufficient mechanical power output to swim to distant food sources and propel themselves to great depth for successful prey capture. To investigate the effects of the annual molt fast on their dive/foraging performance, we studied various dive/foraging parameters and peripheral temperature patterns in immature king penguins across two molt cycles, after birds had spent their first and second year at sea, using implanted data-loggers. We found that the dive/foraging performance of immature king penguins was significantly reduced during post-molt foraging trips. Dive and bottom duration for a given depth were shorter during post-molt and post-dive surface interval duration was longer, reducing overall dive efficiency and underwater foraging time. We attribute this decline to the severe physiological changes that birds undergo during their annual molt. Peripheral temperature patterns differed greatly between pre- and post-molt trips, indicating the loss of the insulating subcutaneous fat layer during molt. Peripheral perfusion, as inferred from peripheral temperature, was restricted to short periods at night during pre-molt but occurred throughout extended periods during post-molt, reflecting the need to rapidly deposit an insulating fat layer during the latter period.

Monocultural sowing in mesocosms decreases the species richness of weeds and invertebrates and critically reduces the fitness of the endangered European hamster.

Intensive cereal monoculture is currently the main cause of biodiversity decline in Europe. However, it is difficult to disentangle the effects of intensive monoculture (e.g. pesticide use, mechanical ploughing and reduced protective cover), let alone evaluate how far the reduction of crop diversity affects biodiversity. It remains unclear to which extent the consequent decrease in food resources affects farmland biodiversity, and particularly vertebrate species. We therefore designed this study in mesocosms to investigate the effects of monoculture crops (organic wheat or corn seeds) and mixed crops (a combination of organic wheat, corn, sunflower and alfalfa seeds) on (1) the species richness of weeds and invertebrates and (2) the reproductive success of the European hamster (Cricetus cricetus), a critically endangered umbrella species of European farmlands. We found a negative impact of organic monoculture crops on plant and invertebrate species richness, with values respectively 38% and 28% lower than those obtained for mixed organic crops. The reproductive success of hamsters was reduced by 82% in monoculture mesocosms. These results highlight that monoculture per se can be detrimental for farmland biodiversity (i.e. from plants to vertebrates), even before taking into account the use of pesticide and mechanization. We believe that future research should further consider how food reduction in agroecosystems affects farmland wildlife, including vertebrates. Moreover, we argue that conservation actions must focus on restoring plant diversity on farmland to reverse the observed trend in farmland wildlife decline.

Diets derived from maize monoculture cause maternal infanticides in the endangered European hamster due to a vitamin B3 deficiency.

From 1735 to 1940, maize-based diets led to the death of hundreds of thousands of people from pellagra, a complex disease caused by tryptophan and vitamin B3 deficiencies. The current cereal monoculture trend restricts farmland animals to similarly monotonous diets. However, few studies have distinguished the effects of crop nutritional properties on the reproduction of these species from those of other detrimental factors such as pesticide toxicity or agricultural ploughing. This study shows that maize-based diets cause high rates of maternal infanticides in the European hamster, a farmland species on the verge of extinction in Western Europe. Vitamin B3 supplementation is shown to effectively restore reproductive success in maize-fed females. This study pinpoints how nutritional deficiencies caused by maize monoculture could affect farmland animal reproduction and hence their fitness.

High peripheral temperatures in king penguins while resting at sea: thermoregulation versus fat deposition.

Marine endotherms living in cold water face an energetically challenging situation. Unless properly insulated, these animals will lose heat rapidly. The field metabolic rate of king penguins at sea is about twice that on land. However, when at sea, their metabolic rate is higher during extended resting periods at the surface than during foraging, when birds descend to great depth in pursuit of their prey. This is most likely explained by differences in thermal status. During foraging, peripheral vasoconstriction leads to a hypothermic shell, which is rewarmed during extended resting bouts at the surface. Maintaining peripheral perfusion during rest in cold water, however, will greatly increase heat loss and, therefore, thermoregulatory costs. Two hypotheses have been proposed to explain the maintenance of a normothermic shell during surface rest: (1) to help the unloading of N2 accumulated during diving; and (2) to allow the storage of fat in subcutaneous tissue, following the digestion of food. We tested the latter hypothesis by maintaining king penguins within a shallow seawater tank, while we recorded tissue temperature at four distinct sites. When king penguins were released into the tank during the day, their body temperature immediately declined. However, during the night, periodic rewarming of abdominal and peripheral tissues occurred, mimicking temperature patterns observed in the wild. Body temperatures, particularly in the flank, also depended on body condition and were higher in 'lean' birds (after 10 days of fasting) than in 'fat' birds. While not explicitly tested, our observation that nocturnal rewarming persists in the absence of diving activity during the day does not support the N2 unloading hypothesis. Rather, differences in temperature changes throughout the day and night, and the effect of body condition/mass supports the hypothesis that tissue perfusion during rest is required for nutritional needs.

Thermal strategies of king penguins during prolonged fasting in water.

Most animals experience periods of unfavourable conditions, challenging their daily energy balance. During breeding, king penguins fast voluntarily for up to 1.5 months in the colony, after which they replenish their energy stores at sea. However, at sea, birds might encounter periods of low foraging profitability, forcing them to draw from previously stored energy (e.g. subcutaneous fat). Accessing peripheral fat stores requires perfusion, increasing heat loss and thermoregulatory costs. Hence, how these birds balance the conflicting demands of nutritional needs and thermoregulation is unclear. We investigated the physiological responses of king penguins to fasting in cold water by: (1) monitoring tissue temperatures, as a proxy of tissue perfusion, at four distinct sites (deep and peripheral); and (2) recording their oxygen consumption rate while birds floated inside a water tank. Despite frequent oscillations, temperatures of all tissues often reached near-normothermic levels, indicating that birds maintained perfusion to peripheral tissues throughout their fasting period in water. The oxygen consumption rate of birds increased with fasting duration in water, while it was also higher when the flank tissue was warmer, indicating greater perfusion. Hence, fasting king penguins in water maintained peripheral perfusion, despite the associated greater heat loss and, therefore, thermoregulatory costs, probably to access subcutaneous fat stores. Hence, the observed normothermia in peripheral tissues of king penguins at sea, upon completion of a foraging bout, is likely explained by their nutritional needs: depositing free fatty acids (FFA) in subcutaneous tissues after profitable foraging or mobilizing FFA to fuel metabolism when foraging success was insufficient.

Apparent changes in body insulation of juvenile king penguins suggest an energetic challenge during their early life at sea.

Little is known about the early life at sea of marine top predators, like deep-diving king penguins (Aptenodytes patagonicus), although this dispersal phase is probably a critical phase in their life. Apart from finding favourable foraging sites, they have to develop effective prey search patterns as well as physiological capacities that enable them to capture sufficient prey to meet their energetic needs. To investigate the ontogeny of their thermoregulatory responses at sea, we implanted 30 juvenile king penguins and 8 adult breeders with a small data logger that recorded pressure and subcutaneous temperature continuously for up to 2.5 years. We found important changes in the development of peripheral temperature patterns of foraging juvenile king penguins throughout their first year at sea. Peripheral temperature during foraging bouts fell to increasingly lower levels during the first 6 months at sea, after which it stabilized. Most importantly, these changes re-occurred during their second year at sea, after birds had fasted for ∼4 weeks on land during their second moult. Furthermore, similar peripheral temperature patterns were also present in adult birds during foraging trips throughout their breeding cycle. We suggest that rather than being a simple consequence of concurrent changes in dive effort or an indication of a physiological maturation process, these seasonal temperature changes mainly reflect differences in thermal insulation. Heat loss estimates for juveniles at sea were initially high but declined to approximately half after ∼6 months at sea, suggesting that juvenile king penguins face a strong energetic challenge during their early oceanic existence.

Reassessment of the cardio-respiratory stress response, using the king penguin as a model.

Research in to short-term cardio-respiratory changes in animals in reaction to a psychological stressor typically describes increases in rate of oxygen consumption (V̇(O2)) and heart rate. Consequently, the broad consensus is that they represent a fundamental stressor response generalizable across adult species. However, movement levels can also change in the presence of a stressor, yet studies have not accounted for this possible confound on heart rate. Thus the direct effects of psychological stressors on the cardio-respiratory system are not resolved. We used an innovative experimental design employing accelerometers attached to king penguins (Aptenodytes patagonicus) to measure and thus account for movement levels in a sedentary yet free-to-move animal model during a repeated measures stress experiment. As with previous studies on other species, incubating king penguins (N = 6) exhibited significant increases in both V̇(O2) and heart rate when exposed to the stressor. However, movement levels, while still low, also increased in response to the stressor. Once this was accounted for by comparing periods of time during the control and stress conditions when movement levels were similar as recorded by the accelerometers, only V̇(O2) significantly increased; there was no change in heart rate. These findings offer evidence that changing movement levels have an important effect on the measured stress response and that the cardio-respiratory response per se to a psychological stressor (i.e. the response as a result of physiological changes directly attributable to the stressor) is an increase in V̇(O2) without an increase in heart rate.

Effect of walking speed on the gait of king penguins: An accelerometric approach.

Little is known about non-human bipedal gaits. This is probably due to the fact that most large animals are quadrupedal and that non-human bipedal animals are mostly birds, whose primary form of locomotion is flight. Very little research has been conducted on penguin pedestrian locomotion with the focus instead on their associated high energy expenditure. In animals, tri-axial accelerometers are frequently used to estimate physiological energy cost, as well as to define the behaviour pattern of a species, or the kinematics of swimming. In this study, we showed how an accelerometer-based technique could be used to determine the biomechanical characteristics of pedestrian locomotion. Eight king penguins, which represent the only family of birds to have an upright bipedal gait, were trained to walk on a treadmill. The trunk tri-axial accelerations were recorded while the bird was walking at four different speeds (1.0, 1.2, 1.4 and 1.6km/h), enabling the amplitude of dynamic body acceleration along the three axes (amplitude of DBAx, DBAy and DBAz), stride frequency, waddling and leaning amplitude, as well as the leaning angle to be defined. The magnitude of the measured variables showed a significant increase with increasing speed, apart from the backwards angle of lean, which decreased with increasing speed. The variability of the measured variables also showed a significant increase with speed apart from the DBAz amplitude, the waddling amplitude, and the leaning angle, where no significant effect of the walking speed was found. This paper is the first approach to describe 3D biomechanics with an accelerometer on wild animals, demonstrating the potential of this technique.

Elevated corticosterone levels and severe weather conditions decrease parental investment of incubating Adélie penguins.

Corticosterone, the main stress hormone in birds, mediates resource allocation, allowing animals to adjust their physiology and behaviour to changes in the environment. Incubation is a time and energy-consuming phase of the avian reproductive cycle. It may be terminated prematurely, when the parents' energy stores are depleted or when environmental conditions are severe. In this study, the effects of experimentally elevated baseline corticosterone levels on the parental investment of incubating male Adélie penguins were investigated. Incubation duration and reproductive success of 60 penguins were recorded. The clutches of some birds were replaced by dummy eggs, which recorded egg temperatures and rotation rates, enabling a detailed investigation of incubation behaviour. Corticosterone levels of treated birds were 2.4-fold higher than those of controls 18 days post treatment. Exogenous corticosterone triggered nest desertion in 61% of the treated birds; consequently reducing reproductive success, indicating that corticosterone can reduce or disrupt parental investment. Regarding egg temperatures, hypothermic events became more frequent and more pronounced in treated birds, before these birds eventually abandoned their nest. The treatment also significantly decreased incubation temperatures by 1.3°C and lengthened the incubation period by 2.1 days. However, the number of chicks at hatching was similar among successful nests, regardless of treatment. Weather conditions appeared to be particularly important in determining the extent to which corticosterone levels affected the behaviour of penguins, as treated penguins were more sensitive to severe weather conditions. This underlines the importance of considering the interactions of organisms with their environment in studies of animal behaviour and ecophysiology.

Decreased prolactin levels reduce parental commitment, egg temperatures, and breeding success of incubating male Adélie penguins.

Hormones regulate many aspects of an individual's phenotype, including various physiological and behavioral traits. Two hormones have been described as important players in the regulation of parental investment in birds: the glucocorticoid hormone corticosterone and prolactin, a pituitary hormone, widely involved in mediating parental behavior. In comparison with corticosterone, the role of prolactin on parental investment remains poorly documented, and most studies so far have been correlative. In this study, the effects of an experimental decrease of prolactin levels on the incubation behavior of a long-lived seabird species were assessed. Male Adélie penguins were treated with self-degradable bromocriptine pellets, inhibiting prolactin secretion. Filming and subsequent video analysis allowed the determination of a behavioral time budget for birds and their position on the nest, while dummy eggs recorded incubation parameters. Incubation duration and breeding success at hatching were also monitored. As expected, bromocriptine-treatment significantly decreased plasma prolactin levels, but did not affect corticosterone levels. The behavioral time budget of penguins was not affected by the treatment. However, treated birds spent significantly more time in an upright position on the nest. These birds also incubated their eggs at lower temperatures and turned their eggs more frequently than controls, resulting in a lengthened incubation period. Despite this, the treatment was insufficient to trigger nest desertion and eggs of treated birds still hatched, indicating that several endocrine signals are required for the induction of nest abandonment. We suggest that the decreased prolactin levels in treated birds offset their timeline of breeding, so that birds displayed behavior typical of early incubation.

Stormwater ponds as an amphibian breeding site: a case study with European green toad tadpoles.

Stormwater ponds (SWPs) are built to collect and retain polluted runoff water from roads. Consequently, they are not perceived as suitable habitat for wetland species, such as many amphibians. However, given the drastic decline of wetland areas, SWPs may serve as a habitat for protected amphibian species, such as the European green toad (Bufotes viridis). The latter species is frequently found inside these artificial ponds, but their reproductive success is unknown. We assessed the suitability of SWPs as breeding habitat for European green toads by monitoring 8 SWPs and 8 semi-natural ponds (SNPs), which served as control sites. At each site, two groups of 30 tadpoles, originating at that site, were held inside two floating enclosures that contained sediment from the respective pond. During bi-weekly monitoring, tadpoles were counted and measured, allowing to estimate growth and mortality rates. A variety of biotic and abiotic factors were studied to determine the causes of potential differences in growth and mortality rates between the two pond types. While growth rate did not differ between pond types, mortality rates were significantly greater in SWPs than in SNPs. The extremely low survival rate observed in SWPs might be explained by the considerably greater pollutant concentration in their sediment and/or by the presence of leeches, which were found exclusively inside SWPs. Implementation of management measures, such as regular draining/dredging during winter, might help to lower the pollutant concentration in the sediment and reduce the density of leeches inside SWPs, improving their suitability as habitat for amphibians.

Improving the success of reinforcement programs: effects of a two-week confinement in a field enclosure on the anti-predator behaviour of captive-bred European hamsters.

Captive breeding programs are an important pillar in biodiversity conservation, aiming to prevent the extinction of threatened species. However, the establishment of self-sustaining populations in the wild through the release of captive-bred animals is often hampered by a high mortality upon release. In this study, we investigated how a 2-week confinement period within a large field enclosure affected the anti-predator behaviour of 'naive' captive-bred hamsters and how potential modifications persisted over time. During three consecutive tests, hamsters were confronted with a moving predator model (a red fox mount, Vulpes vulpes) and their behaviour was filmed. After the initial round of confrontation with the predator model, one group of hamsters (field group) was released into a field enclosure protected from predators, while the other group (control) remained in their individual laboratory cages. After 2 weeks, hamsters from the field group were recaptured and individuals of both groups underwent a second confrontation test. A total of 1 month after their return from the field enclosure, field hamsters were subjected to a last confrontation test. Video analysis, investigating four behavioural variables, revealed that field hamsters significantly modified their behavioural response following the 2 weeks confinement in the enclosure, while this was not the case for control hamsters. In addition, most behavioural modifications in field hamsters persisted over 1 month, while others started to revert. We suggest that an appropriate pre-release period inside a field enclosure will enable naive (captive-bred) hamsters to develop an adequate anti-predator behaviour that will increase their immediate survival probability upon release into the wild. We believe that such measure will be of great importance for hamster conservation programs.

Similar circling movements observed across marine megafauna taxa.

Advances in biologging technology have enabled 3D dead-reckoning reconstruction of marine animal movements at spatiotemporal scales of meters and seconds. Examining high-resolution 3D movements of sharks (Galeocerdo cuvier, N = 4; Rhincodon typus, N = 1), sea turtles (Chelonia mydas, N = 3), penguins (Aptenodytes patagonicus, N = 6), and marine mammals (Arctocephalus gazella, N = 4; Ziphius cavirostris, N = 1), we report the discovery of circling events where animals consecutively circled more than twice at relatively constant angular speeds. Similar circling behaviors were observed across a wide variety of marine megafauna, suggesting these behaviors might serve several similar purposes across taxa including foraging, social interactions, and navigation.

Measuring foraging activity in a deep-diving bird: comparing wiggles, oesophageal temperatures and beak-opening angles as proxies of feeding.

Quantification of prey consumption by marine predators is key to understanding the organisation of ecosystems. This especially concerns penguins, which are major consumers of southern food webs. As direct observation of their feeding activity is not possible, several indirect methods have been developed that take advantage of miniaturised data logging technology, most commonly: detection of (i) anomalies in diving profiles (wiggles), (ii) drops in oesophageal temperature and (iii) the opening of mouth parts (recorded with a Hall sensor). In the present study, we used these three techniques to compare their validity and obtain information about the feeding activity of two free-ranging king penguins (Aptenodytes patagonicus). Crucially, and for the first time, two types of beak-opening events were identified. Type A was believed to correspond to failed prey-capture attempts and type B to successful attempts, because, in nearly all cases, only type B was followed by a drop in oesophageal temperature. The number of beak-opening events, oesophageal temperature drops and wiggles per dive were all correlated. However, for a given dive, the number of wiggles and oesophageal temperature drops were lower than the number of beak-opening events. Our results suggest that recording beak opening is a very accurate method for detecting prey ingestions by diving seabirds at a fine scale. However, these advantages are counterbalanced by the difficulty, and hence potential adverse effects, of instrumenting birds with the necessary sensor/magnet, which is in contrast to the less accurate but more practicable methods of measuring dive profiles or, to a lesser extent, oesophageal temperature.

Why implantation of bio-loggers may improve our understanding of how animals cope within their natural environment.

Bio-loggers are miniaturized autonomous devices that record quantitative data on the state of free-ranging animals (e.g. behavior, position and physiology) and their natural environment. This is especially relevant for species where direct visual observation is difficult or impossible. Today, ongoing technical development allows the monitoring of numerous parameters in an increasing range of species over extended periods. However, the external attachment of devices might affect various aspects of animal performance (energetics, thermoregulation, foraging as well as social and reproductive behavior), which ultimately affect fitness. External attachment might also increase entanglement risk and the conspicuousness of animals, leaving them more vulnerable to predation. By contrast, implantation of devices can mitigate many of these undesirable effects and might be preferable, especially for long-term studies, provided that the many challenges associated with surgical procedures can be mastered. Implantation may then allow us to gather data that would be impossible to obtain otherwise and thereby may provide new and ecologically relevant insights into the life of wild animals. Here, we: (i) discuss the pros and cons of attachment methods; (ii) highlight recent field studies that used implanted bio-loggers to address eco-physiological questions in a wide range of species; and (iii) discuss logger implantation in light of ethical considerations.

Captive-reared European hamsters follow an offensive strategy during risk-assessment.

Understanding whether captive-reared animals destined to reintroduction are still able to discriminate predators has important implications for conservation biology. The endangered European hamster benefits from conservation programs throughout Europe, in which several thousand individuals are released into the wild every year. Despite this, the anti-predator strategy of hamsters and their ability to maintain predator discrimination in captivity remain to be investigated. Here, we explore the predator discrimination behaviour of captive-reared European hamsters and their response to different predation cues. When first exposed to the urine of cats and goats in a Y-maze test, hamsters spent more time close to the cat scent rather than to the goat scent. In a second experiment, during which hamsters were exposed to a non-mobile European ferret (inside a cage), hamsters significantly increased the time spent close to the ferret's cage and displayed aggressive behaviour towards the ferret. Furthermore, they did not take refuge inside an anti-predation tube (APT), a device designed to upgrade wildlife underpasses and reconnect wild hamster populations. Finally, when exposed to a mobile ferret (but without physical contact), hamsters displayed mobbing and aggressive behaviours towards the ferret, before taking refuge inside the APT. Taken together, our results show that captive-reared hamsters are still able to detect and react to predation cues, but that they initially adopt an offensive strategy (grunting, spitting, mobbing) during the risk-assessment phase. After risk assessment, however, hamsters used the APT as a refuge. Our study provides important insights into the anti-predator behaviour of hamsters. Testing the efficacy of the APT, a device that will allow upgrading wildlife underpasses for the hamster and other rodents, is also of great importance and is instrumental in conservation efforts for these species.

Dive and beak movement patterns in leatherback turtles Dermochelys coriacea during internesting intervals in French Guiana.

1. Investigating the foraging patterns of free-ranging species is essential to estimate energy/time budgets for assessing their real reproductive strategy. Leatherback turtles Dermochelys coriacea (Vandelli 1761), commonly considered as capital breeders, have been reported recently to prospect actively during the breeding season in French Guiana, Atlantic Ocean. In this study we investigate the possibility of this active behaviour being associated with foraging, by studying concurrently diving and beak movement patterns in gravid females equipped with IMASEN (Inter-MAndibular Angle SENsor). 2. Four turtles provided data for periods varying from 7.3 to 56.1 h while exhibiting continuous short and shallow benthic dives. Beak movement ('b-m') events occurred in 34% of the dives, on average 1.8 +/- 1.4 times per dive. These b-m events lasted between 1.5 and 20 s and occurred as isolated or grouped (two to five consecutive beak movements) events in 96.0 +/- 4.0% of the recorded cases, and to a lesser extent in series (> five consecutive beak movements). 3. Most b-m events occurred during wiggles at the bottom of U- and W-shaped dives and at the beginning and end of the bottom phase of the dives. W-shaped dives were associated most frequently with beak movements (65% of such dives) and in particular with grouped beak movements. 4. Previous studies proposed wiggles to be indicator of predatory activity, U- and W-shaped dives being putative foraging dives. Beak movements recorded in leatherbacks during the first hours of their internesting interval in French Guiana may be related to feeding attempts. 5. In French Guiana, leatherbacks show different mouth-opening patterns for different dive patterns, suggesting that they forage opportunistically on occasional prey, with up to 17% of the dives appearing to be successful feeding dives. 6. This study highlights the contrasted strategies adopted by gravid leatherbacks nesting on the Pacific coasts of Costa Rica, in the deep-water Caribbean Sea and in the French Guianan shallow continental shelf, and may be related to different local prey accessibility among sites. Our results may help to explain recently reported site-specific individual body size and population dynamics.

Pressure equilibration in the penguin middle ear.

CONCLUSIONS: King penguins have a venous structure in the form of a corpus cavernosum (CC) in their middle ear (ME) submucosa. The CC may be viewed as a special organelle that can change ME volume for pressure equilibration during deep-sea diving it is a pressure regulating organelle (PRO). A similar CC and muscles also surround the external ear (EE) and may constrict it, isolating the tympanic membrane from the outside. A CC was previously found also in the ME of marine diving mammals and can be expected to exist in other deep diving animals, such as marine turtles. OBJECTIVES: Marine animals require equalization of middle ear (ME) pressure when diving hundreds or thousands of meters to catch prey. We investigated what mechanism enables king penguins to protect their ME when they dive to great depths. MATERIALS AND METHODS: Biopsies and serial sections of the ME and the EE of the deep diving king penguin (Aptenodytes patagonicus) were examined microscopically. RESULTS: It was demonstrated that the penguin ME has an extensive network of small and large submucosal venous sinuses. This venous formation, a corpus cavernosum, can expand and potentially 'flood' the ME almost completely on diving, thus elevating ME pressure and reducing the ME space. The EE has a similar protective mechanism.

Stroke frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans.

It is obvious, at least qualitatively, that small animals move their locomotory apparatus faster than large animals: small insects move their wings invisibly fast, while large birds flap their wings slowly. However, quantitative observations have been difficult to obtain from free-ranging swimming animals. We surveyed the swimming behaviour of animals ranging from 0.5 kg seabirds to 30 000 kg sperm whales using animal-borne accelerometers. Dominant stroke cycle frequencies of swimming specialist seabirds and marine mammals were proportional to mass(-0.29) (R(2)= 0.99, n = 17 groups), while propulsive swimming speeds of 1-2 m s(-1) were independent of body size. This scaling relationship, obtained from breath-hold divers expected to swim optimally to conserve oxygen, does not agree with recent theoretical predictions for optimal swimming. Seabirds that use their wings for both swimming and flying stroked at a lower frequency than other swimming specialists of the same size, suggesting a morphological trade-off with wing size and stroke frequency representing a compromise. In contrast, foot-propelled diving birds such as shags had similar stroke frequencies as other swimming specialists. These results suggest that muscle characteristics may constrain swimming during cruising travel, with convergence among diving specialists in the proportions and contraction rates of propulsive muscles.