The development of diving in marine endotherms: preparing the skeletal muscles of dolphins, penguins, and seals for activity during submergence

Myoglobin is an important oxygen store for supporting aerobic diving in endotherms, yet little is known about its role during postnatal development. Therefore, we compared the postnatal development of myoglobin in marine endotherms that develop at sea (cetaceans) to those that develop on land (penguins and pinnipeds). We measured myoglobin concentrations in the major locomotor muscles of mature and immature bottlenose dolphins (Tursiops truncatus) and king penguins (Aptenodytes patagonicus) and compared the data to previously reported values for northern elephant seals (Mirounga angustirostris). Neonatal dolphins, penguins, and seals lack the myoglobin concentrations required for prolonged dive durations, having 10%, 9%, and 31% of adult values, respectively. Myoglobin contents increased significantly during subsequent development. The increases in myoglobin content with age may correspond to increases in activity levels, thermal demands, and time spent in apnea during swimming and diving. Across these phylogenetically diverse taxa (cetaceans, penguins, and pinnipeds), the final stage of postnatal development of myoglobin occurs during the initiation of independent foraging, regardless of whether development takes place at sea or on land.     

Comparison of foraging strategies of incubating king penguins Aptenodytes patagonicus from Macquarie and Heard islands

The foraging strategies of king penguins from Heard and Macquarie islands were compared using satellite telemetry, time-depth recorders and diet samples. Trip durations were 16.8±3.6 days and 14.8±4.1 days at Macquarie and Heard islands, respectively. At Macquarie Island, total distances travelled were 1281±203 km compared to 1425±516 km at Heard Island. The total time the penguins spent at sea was 393±66 h at Macquarie Island and 369±108 h at Heard Island. The penguins from Macquarie Island performed more deep dives than those from Heard Island. King penguins from Macquarie Island travelled 1.5±0.2 km h⁻¹ day⁻¹ compared to 1.3±0.1 km h⁻¹ day⁻¹. At Macquarie Island, 19% of dives were upto 70–90 m depth compared to 35% at Heard Island. The main dietary prey species were the fish Krefftychthis anderssoni and the squid Moroteuthis ingens in both groups. The differences in the at-sea distribution and the foraging behaviour of the two groups of penguins were possibly related to differences in oceanography and bathymetric conditions around the two islands. Dietary differences may be due to interannual variability in prey availability since the two colonies were studied during incubation but in different years.     

Corticosterone predicts foraging behavior and parental care in macaroni penguins

Corticosterone has received considerable attention as the principal hormonal mediator of allostasis or physiological stress in wild animals. More recently, it has also been implicated in the regulation of parental care in breeding birds, particularly with respect to individual variation in foraging behavior and provisioning effort. There is also evidence that prolactin can work either inversely or additively with corticosterone to achieve this. Here we test the hypothesis that endogenous corticosterone plays a key physiological role in the control of foraging behavior and parental care, using a combination of exogenous corticosterone treatment, time-depth telemetry, and physiological sampling of female macaroni penguins (Eudyptes chrysolophus) during the brood-guard period of chick rearing, while simultaneously monitoring patterns of prolactin secretion. Plasma corticosterone levels were significantly higher in females given exogenous implants relative to those receiving sham implants. Increased corticosterone levels were associated with significantly higher levels of foraging and diving activity and greater mass gain in implanted females. Elevated plasma corticosterone was also associated with an apparent fitness benefit in the form of increased chick mass. Plasma prolactin levels did not correlate with corticosterone levels at any time, nor was prolactin correlated with any measure of foraging behavior or parental care. Our results provide support for the corticosterone-adaptation hypothesis, which predicts that higher corticosterone levels support increased foraging activity and parental effort.     

Non-consumptive factors affecting foraging patterns in Antarctic penguins: a review and synthesis

Recent research has clearly shown that the fear of predation, i.e. aversion to taking risks, among mesopredators or grazers, and not merely flight from an apex predator to avoid predation, is an important aspect of ecosystem structuring. In only a few, though well-documented cases, however, has this been considered in the marine environment. Herein, we review studies that have quantified behavioral responses of Adélie penguins Pygoscelis adeliae and emperor penguins Aptenodytes forsteri to the direct presence of predators, and question why the penguins avoid entering or exiting the water at night. We also show, through literature review and new analyses of Adélie penguin diving data, that Antarctic penguins are capable of successful prey capture in the dark (defined here as <3.4 lux). Finally, we summarize extensive data on seasonal migration relative to darkness and prey availability. On the basis of our findings, we propose that penguins’ avoidance of foraging at night is due to fear of predation, and not to an inability to operate effectively in darkness. We further propose that, at polar latitudes where darkness is more a seasonal than a year-round, daily feature, this “risk aversion” affects migratory movements in both species, consistent with the “trade-off” hypothesis seen in other marine vertebrates weighing foraging success against predation risk in their choice of foraging habitat. Such non-consumptive, behavioral aspects of species interactions have yet to be considered as important in Southern Ocean food webs, but may help to explain enigmatic movement patterns and choice of foraging grounds in these penguin species.     

Stable isotopes in southern rockhopper penguins: foraging areas and sexual differences in the non-breeding period

Southern rockhopper penguins (Eudyptes chrysocome chrysocome) have experienced severe population declines across their distribution area, potentially in response to bottom-up effects following elevated sea surface temperatures, changes in the food web and prey availability. We conducted stable isotope analysis to compare trophic levels and distribution patterns in the non-breeding period over three consecutive years, and between males and females, using egg membranes, blood cells and feathers of parent birds. Tissues representing the non-breeding season had lower ??¹³C values than prey sampled around the Falklands and red blood cells from breeding rockhopper penguins. In contrast, ??¹⁵N values were higher in red blood cells from the end of winter compared to those from the breeding season and compared to feathers. This indicated that rockhopper penguins left the Falkland Island area in the non-breeding season and foraged either around Burdwood Bank further south, or over the Patagonian Shelf. In winter, only males took more prey of higher trophic level than females. Inter-annual differences in isotopic values partly correlated with sea surface temperatures. However, as prey isotope samples were collected only in 1?year, inter-annual differences in penguin isotopic values may result from different foraging sites, different prey choice or different isotopic baseline values. Our study highlights the potential for stable isotope analyses to detect seasonal and gender-specific differences in foraging areas and trophic levels, while stressing the need for more sampling of isotopic baseline data.     

Pre-moult foraging trips and moult locations of Emperor penguins at the Mawson Coast

The movements of nine breeding adult emperor penguins Aptenodytes forsteri from two colonies, Auster (67° 23S 64° 04E) and Taylor Glacier (67° 28S 60° 54E), were determined by satellite telemetry on their pre-moult foraging trips. While preparing for their annual moult the penguins travelled for 22–38 days and reached distances of up to 618 km from the colony. Six of the nine tracked penguins were followed to three different moult locations all to the west of their breeding colonies and near other known emperor penguins colonies, such as Kloa Point (66°38S, 59°23E) and Fold Island (67°17S, 59°23E). Sea-ice conditions changed throughout the tracking period; as the birds travelled north the sea-ice contracted south.     

Optimal foraging in patches: A case for stochasticity

Like much mathematical modeling in biology, most optimal foraging theory is developed from deterministic analogs of basically stochastic processes. Unlike other models, however, it cannot depend on laws of large numbers to justify this simplification; ignoring stochasticity can lead to wrong answers. This is demonstrated for a predator searching spatially separated patches of prey; it is shown that the choice of an optimal procedure for deciding when to leave a patch must be based on a stochastic model—a predator whose procedure is based on a deterministic model can do arbitrarily badly by comparison with the stochastic optimizer. A general solution is given, and its complexity suggests some objections to standard optimality arguments, and some possible alternatives.     

Optimal foraging: A case for random movement

Summary The bumblebee, Bombus flavifrons, forages randomly with respect to direction on Polemonium foliosissimum. This foraging pattern is as predicted for a system where there is a low probability of revisiting any given flower upon returning to a patch. This low revisitation probability is a function of the floral resource arrangement. It is further shown that B. flavifrons is using the resource distribution to direct its movements. A large percentage of all movements are to nearest neighbors with maximal foraging efficiency gained through minimization of flight distances.     

Seasonal change in foraging areas and dive depths of breeding king penguins at Heard Island

The seasonal variation in the foraging behaviour of king penguins (Aptenodytes patagonicus) was studied at Heard Island (53°05′S, 73°30′E) during 1992/1993. On seven occasions throughout the breeding cycle, time-depth-light recorders were deployed on breeding adults to record the dive activities and foraging. Foraging locations changed with season: in autumn and spring 1992, adults foraged between 48–52°S and 74–78°E, about 370 km NNE of Heard Island close to the Polar Front. Two penguins tracked in winter travelled 2220 km east of Heard Island (95°E) along the northern ice limit, and 1220 km south of Heard Island to approximately 65°S, respectively. In spring (October), the penguins again foraged further north than during winter. The foraging area utilised in October overlapped the area where the penguins foraged in March/April. The penguins' diving behaviour also varied seasonally: the modal depth of deep dives (>50 m) increased from about 100 m in February to 220 m in October. Mean dive depths increased from 70 ± 52 m in March 1992 to 160 ± 68 m in August 1992. Penguins dived deep (>50 m) only during daylight hours (16 h in February, 9 h in July). Mean dive durations ranged from 2.9 ± 1.1 min in March 1992 to 5.1 ± 1.2 min in August 1992. Associated with changes in foraging location and dive behaviour was a change in diet composition: during summer the penguins ingested mainly myctophid fish (>90%) while in winter the most important diet item was squid. Accepted: 19 October 1998     

Parallels between the foraging strategies of ants and plants

Animal and plant ecologists generally follow separate paths. This often leads to disjointed approaches to solving similar ecological problems. In the past 20 years, two related, but unconnected, research fields have undergone rapid development: modular demography, with its morphological and functional analysis of resource capture, until now basically the domain of plant ecology; and foraging theory, traditionally applied and developed in animal ecology. The results of recent research on the foraging strategies of ants and clonal plants, however, outline a general framework of functional parallels between both types of organisms that could link important aspects of animal and plant foraging ecology.     

Harvest rates and foraging strategies in Negev Desert gerbils

We examined the foraging strategy and quantified the foragingtraits of two nocturnal rodent species, Allenby's gerbil (Gerbillusallenbyi) and the greater Egyptian sand gerbil (Gerbillus pyramidum).In the laboratory, both species used two distinct foragingstrategies: either they immediately consumed seeds found ina patch (seed tray); or they collected and delivered the seedsto their nest box for later consumption. Moreover, we founda transition in foraging strategy among individual G. allenbyi under laboratory conditions; they all began by consuming theseeds on the tray and, after 7 days on average, switched tothe collecting strategy. By contrast, in the field both speciesused only one foraging strategy; they collected and deliveredthe seeds to their burrow or to surface caches for later consumption.Furthermore, G. allenbyi and G. pyramidum collected seeds atsignificantly higher rates in the field than in the laboratorybecause the seed encounter rates for both species were higherin the field. This suggests that in natural conditions, probablyinvolving predation risk and competitive pressure, gerbilsmust respond in two ways: (1) they must choose a foraging strategythat reduces predation risk by minimizing time spent feedingoutside their burrows; and (2) they must forage more efficiently.In the field, seed handling time of the larger species, G. pyramidum, was shorter than that of the smaller one, G. allenbyi.This difference may give G. pyramidum an advantage when resourcelevels are high and when most of a forager's time is spent handling seeds rather than searching for more seeds. Additionally,our field study showed that the seed encounter rate of G. allenbyiwas higher than that of G. pyramidum. This difference may giveG. allenbyi an advantage when resource levels are low and whensearching occupies most of the forager's time. The differentadvantages that each species has over the other, under differentconditions, may well be factors promoting their coexistenceover a wide range of resource densities.     

Optimal foraging: the difficulty of exploiting different feeding strategies simultaneously

Summary The foraging efficiency of a visually feeding fish, perch (Perca fluviatilis) was studied on two prey species (Daphnia magna and Chaoborus obscuripus) presented either separately or combined. It is shown that when both prey species are present, the foraging efficiency of the predator is reduced. This is due to the predator's inability to simultaneously cope with prey species with different anti-predatory behaviour. In the mixed-meal experiment the predator captured both prey species in equal proportions in disagreement with optimal foraging models assuming that handling time and encounter rate for a prey species are independent of other prey species. The results are, however, in agreement with optimal foraging models assuming that handling time and encounter rate are influenced by short time learning.     

A life in the fast lane: energetics and foraging strategies of the great cormorant

Body insulation is critically important for diving marine endotherms. However,cormorants have a wettable plumage, which leads to poor insulation. Despitethis, these birds are apparently highly successful predatorsin most aquatic ecosystems. We studied the theoretical influenceof water temperature, dive depth, foraging techniques, and preyavailability on the energetic costs of diving, prey search time,daily food intake, and survival in foraging, nonbreeding greatcormorants (Phalacrocorax carbo). Our model was based on fieldmeasurements and on data taken from the literature. Water temperatureand dive depth influenced diving costs drastically, with predicted increasesof up to 250% and 258% in males and females, respectively. Changes inwater temperature and depth conditions may lead to an increaseof daily food intake of 500-800 g in males and 440-780 g infemales. However, the model predicts that cormorant foragingparameters are most strongly influenced by prey availability,so that even limited reduction in prey density makes birds unableto balance energy needs and may thus limit their influence onprey stocks. We discuss the ramifications of these results withregard to foraging strategies, dispersal, population dynamics,and intraspecific competition in this avian predator and pointout the importance of this model species for our understandingof foraging energetics in diving endotherms.     

Thermal and digestive constraints to foraging behaviour in marine mammals

While foraging models of terrestrial mammals are concerned primarily with optimizing time/energy budgets, models of foraging behaviour in marine mammals have been primarily concerned with physiological constraints. This has historically centred on calculations of aerobic dive limits. However, other physiological limits are key to forming foraging behaviour, including digestive limitations to food intake and thermoregulation. The ability of an animal to consume sufficient prey to meet its energy requirements is partly determined by its ability to acquire prey (limited by available foraging time, diving capabilities and thermoregulatory costs) and process that prey (limited by maximum digestion capacity and the time devoted to digestion). Failure to consume sufficient prey will have feedback effects on foraging, thermoregulation and digestive capacity through several interacting avenues. Energy deficits will be met through catabolism of tissues, principally the hypodermal lipid layer. Depletion of this blubber layer can affect both buoyancy and gait, increasing the costs and decreasing the efficiency of subsequent foraging attempts. Depletion of the insulative blubber layer may also increase thermoregulatory costs, which will decrease the foraging abilities through higher metabolic overheads. Thus, an energy deficit may lead to a downward spiral of increased tissue catabolism to pay for increased energy costs. Conversely, the heat generated through digestion and foraging activity may help to offset thermoregulatory costs. Finally, the circulatory demands of diving, thermoregulation and digestion may be mutually incompatible. This may force animals to alter time budgets to balance these exclusive demands. Analysis of these interacting processes will lead to a greater understanding of the physiological constraints within which the foraging behaviour must operate.