Diving behaviour differs between incubating and brooding Brünnich's guillemots, Uria lomvia

Bird-borne data loggers were used to investigate the foraging strategies of Brünnich's guillemots breeding in a colony in the North Water Polynya: the flight performance and diving activity of incubating birds were compared to those of chick-rearing individuals. No significant differences were recorded between the bird groups in the potential foraging range. Conversely, clear differences were revealed between incubating and chick-rearing birds in diving behaviour. Chick-rearing birds were generally foraging at a significantly greater depth, and spent significantly higher proportions of the time submerged, than brooding individuals. Despite these differences, the estimated average daily energy expenditure of chick-rearing Brünnich's guillemots was only about 6% higher than that during incubation.     

Effects of back-mounted biologgers on condition,diving and flight performance in a breeding seabird

Biologging devices are providing detailed insights into the behaviour and movement of animals in their natural environments. It is usually assumed that this method of gathering data does not impact on the behaviour observed. However, potential negative effects on birds have rarely been investigated before field-based studies are initiated. Seabirds which both fly and use pursuit diving may be particularly sensitive to increases in drag and load resulting from carrying biologging devices. We studied chick-rearing adult common guillemots Uria aalge equipped with and without back-mounted GPS tags over short deployments of a few days. Concurrently guillemots carried small leg-mounted TDR devices (time-depth recorders) providing activity data throughout. Changes in body mass and breeding success were followed for device equipped and control guillemots. At the colony level guillemots lost body mass throughout the chick-rearing period. When-equipped with the additional GPS tag, the guillemots lost mass at close to twice the rate they did when equipped with only the smaller leg-mounted TDR device. The elevated mass loss suggests an impact on energy expenditure or foraging performance. When equipped with GPS tags diving performance, time-activity budgets and daily patterns of activity were unchanged, yet dive depth distributions differed. We review studies of tag-effects in guillemots Uria sp. finding elevated mass loss and reduced chick-provisioning to be the most commonly observed effects. Less information is available for behavioural measures, and results vary between studies. In general, small tags deployed over several days appear to have small or no measurable effect on the behavioural variables commonly observed in most guillemot tagging studies. However, there may still be impacts on fitness via physiological effects and/or reduced chick-provisioning, while more detailed measures of behaviour (e.g. using accelerometery) may reveal effects on diving and flight performance.     

Water temperature sampling by foraging Brünnich's Guillemots with bird-borne data loggers

We describe the features of waters where seabirds were feeding by sampling vertical water temperature profiles with data loggers mounted on five Brünnich's Guillemots in Svalbard, Norway. The guillemots foraged in a cold water (−0.5–0.5°C SST (sea surface temperature)) by making 1.8 dive bouts in short trips (32–257 min duration) as well as in moderate (0.5–2.0°C SST) and warm waters (2.5–4.0°C SST) by making 6.0 dive bouts during long trips (411–688 min duration). Judging from outbound flying time (15.7–24.4 min), time between dive bouts (23.9–43.3 min) and water types, the birds probably fed in fjord or coastal waters during short trips and in both coastal and offshore waters during long trips. Water temperature and diving behaviour can be simultaneously recorded by small data loggers, which therefore will provide useful information on marine features and foraging activity of top predators.     

Brünnich's guillemots (Uria lomvia) maintain high temperature in the body core during dives

A major challenge for diving birds, reptiles, and mammals is regulating body temperature while conserving oxygen through a reduction in metabolic processes. To gain insight into how these needs are met, we measured dive depth and body temperatures at the core or periphery between the skin and abdominal muscles simultaneously in freely diving Brünnich's guillemots (Uria lomvia), an arctic seabird, using an implantable data logger (16-mm diameter, 50-mm length, 14-g mass, Little Leonardo Ltd., Tokyo). Guillemots exhibited increased body core temperatures, but decreased peripheral temperatures, during diving. Heat conservation within the body core appeared to result from the combined effect of peripheral vasoconstriction and a high wing beat frequency that generates heat. Conversely, the observed tissue hypothermia in the periphery should reduce metabolic processes as well as heat loss to the water. These physiological effects are likely one of the key physiological adaptations that makes guillemots to perform as an efficient predator in arctic waters.     

Effects of body size,sex, parental care and moult strategies on auk diving behaviour outside the breeding season

Information on seabird foraging behaviour outside the breeding season is currently limited. This knowledge gap is critical as this period is energetically demanding due to post‐fledging parental care, feather moult and changing environmental conditions. Based on species’ body size, post‐fledging parental strategy and primary moult schedule we tested predictions for key aspects of foraging behaviour (maximum dive depth (MDD), daily time submerged (DTS) and diurnal dive activity (DDA)) using dive depth data collected from three seabird species (common guillemot Uria aalge, razorbill Alca torda and Atlantic puffin Fratercula arctica) from the end of the breeding season (July) to mid‐winter (January). We found partial support for predictions associated with body size; guillemots had greater MDD than razorbills but MDD did not differ between razorbills and puffins, despite the former being 35% heavier. In accordance with sexual monomorphism in all three species, MDD did not differ overall between the sexes. However, in guillemots and razorbills there were sex‐specific differences, such that male guillemots made deeper dives than females, and males of both species had higher DTS. In contrast, there were no marked sex differences in dive behaviour of puffins in July and August in accordance with their lack of post‐fledging parental care and variable moult schedule. We found support for the prediction that diving effort would be greater in mid‐winter compared to the period after the breeding season. Despite reduced daylight in mid‐winter, this increase in DTS occurred predominantly during the day and only guillemots appeared to dive nocturnally to any great extent. In comparison to diving behaviour of these species recorded during the breeding season, MDD was shallower and DTS was greater during the non‐breeding period. Such differences in diving behaviour during the post‐breeding period are relevant when identifying potential energetic bottlenecks, known to be key drivers of seabird population dynamics.     

The influence of temperature on diving behaviour in the alpine newt, Triturus alpestris

An aquatic lifestyle poses serious restriction to air-breathing animals in terms of time and energy spent during a dive cycle. The diving frequency increases with water temperature, therefore an ectotherm's time budget greatly depends on the thermal characteristics of the aquatic environment. Available data suggests that time costs caused by temperature-dependent dive frequency can be partially compensated for by adjusting the swimming speed and diving angle during dive cycle. We tested this prediction by examining the influence of temperature on the diving behaviour of the alpine newt, Triturus alpestris. The ascending speed and angle showed disparate patterns of temperature dependency, with a minor influence on travel duration. Surprisingly, at higher temperatures, the diving newts saved most of their time by restricting swimming activity in the water column during their return to the bottom and not by adjusting their ascending duration. Hence, aquatic newts have the capacity to reduce temperature-dependent time costs of aerial breathing primarily by behavioural modifications during the descending phase of the dive cycle.     

Optimal diving under the risk of predation

Many air-breathing aquatic foragers may be killed by aerial or subsurface predators while recovering oxygen at the surface; yet the influence of predation risk on time allocation during dive cycles is little known in spite of numerous studies on optimal diving. We modeled diving behavior under the risk of predation at the surface. The relationship between time spent at the surface and the risk of death is predicted to influence the optimal surface interval, regardless of whether foragers accumulate energy at a constant rate while at the food patch, deplete food resources over the course of the dive, or must search for food during the dive. When instantaneous predation risk during a single surface interval decreases with time spent at the surface, a diver should increase its surface interval relative to that which maximizes energy intake, thereby increasing dive durations and reducing the number of surfacings per foraging bout. When instantaneous risk over a single surface interval does not change or increases with increasing time at the surface, divers should decrease their surface interval (and consequently their dive duration) relative to that which maximizes energy intake resulting in more dives per foraging bout. The fitness consequences of selecting a suboptimal surface interval vary with the risk function and the way divers harvest energy when at depth. Finally, predation risk during surface intervals should have important consequences for habitat selection and other aspects of the behavioral ecology of air-breathing aquatic organisms.     

The diving behaviour of the Manx Shearwater Puffinus puffinus

The diving capabilities of the Procellariformes remain the least understood component of avian diving physiology. Due to their relatively small size, shearwaters may have high oxygen consumption rates during diving relative to their available oxygen stores. Dive performance in this group should be strongly limited by the trade‐off between oxygen consumption and oxygen stores, and shearwaters could be a good model group for testing predictions of dive theory. Many earlier measurements of shearwater dive behaviour relied on observations from the surface or potentially biased technology, and it is only recently that diving behaviour has been observed using electronic recorders for many of the clades within the family. The diving behaviour of Manx Shearwaters Puffinus puffinus breeding in Wales, UK, was studied on a large sample of birds using time–depth–temperature recorders deployed on chick‐rearing shearwaters in July and August over 3 years (2009–2011). Light availability apparently limited diving as dives only occurred between 04:00 and 19:00 h GMT. All individuals routinely dived deeper than traditionally assumed, to a mean maximum depth of 31 m and occasionally down to nearly 55 m. We compiled all available data for a comparison of the dive depth across shearwater species. There was a positive allometric relationship between maximum dive depth and body mass across Puffinus and Ardenna shearwater species, as expected, but only if samples of fewer than two individuals were excluded. The large intra‐specific range in maximum dive depth in our study illustrates that apparent diversity in diving performance across species must be interpreted cautiously.     

Effects of prey abundance on the foraging behaviour, diving efficiency and time allocation of breeding Guillemots Uria aalge

The foraging behaviour of Guillemots Uria aalge at sea was compared between 2 years of radically different food abundance. Radio telemetry was used to determine foraging locations and diving patterns. In the poor compared with the good food year, foraging trips were much longer, the birds foraged more than six times further from their breeding sites, they spent over five times as much time diving when at sea and their estimated energy expenditure was twice as great. Time spent foraging in the poor food year was at the expense of time spent sitting at the colony. The duration of a foraging trip was a poor indicator of distance travelled but a good indicator of the amount of time spent diving. Mean dive durations, surface pause durations and interbout periods did not differ between years, but individuals made more than four times as many dives per diving bout in the poor food year. Surface pause lengths did not vary with water depth in either year. In the poor food year, birds made shorter surface pauses for a dive of a gi^ven duration than in the good food year, possibly accepting a lactic acid debt in order to maximize searching time, The duration of the interbout period was positively related to the number of dives in the previous bout, and dives tended to get shorter in long diving sequences, suggesting possible exhaustion effects. These data demonstrate that breeding Guillemots have the capacity to adjust their foraging behaviour and time budgets in response to changes in food abundance, but this flexibility was not sufficient to compensate fully for the very low food abundance experienced by birds in this study.     

Stroke and glide of wing-propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth

In order to increase locomotor efficiency, breath-holding divers are expected to adjust their forward thrusts in relation to changes of buoyancy with depth. Wing propulsion during deep diving by Brünnich's guillemots (Uria lomvia) was measured in the wild by high-speed (32 Hz) sampling of surge (tail-to-head) and heave (ventral-to-dorsal) accelerations with bird-borne data loggers. At the start of descent, the birds produced frequent surges (3.2 Hz) during both the upstroke and the downstroke against buoyancy to attain a mean speed of 1.2-1.8 m s(-1) that was close to the expected optimal swim speed. As they descended deeper, the birds decreased the frequency of surges to 2.4 Hz, relaying only on the downstroke. During their ascent, they stopped stroking at 18 m depth, after which the swim speed increased to 2.3 m s(-1), possibly because of increasing buoyancy as air volumes expanded. This smooth change of surge frequency was achieved while maintaining a constant stroke duration (0.4-0.5 s), presumably allowing efficient muscle contraction.     

Utilisation of Intensive Foraging Zones by Female Australian Fur Seals

Within a heterogeneous environment, animals must efficiently locate and utilise foraging patches. One way animals can achieve this is by increasing residency times in areas where foraging success is highest (area-restricted search). For air-breathing diving predators, increased patch residency times can be achieved by altering both surface movements and diving patterns. The current study aimed to spatially identify the areas where female Australian fur seals allocated the most foraging effort, while simultaneously determining the behavioural changes that occur when they increase their foraging intensity. To achieve this, foraging behaviour was successfully recorded with a FastLoc GPS logger and dive behaviour recorder from 29 individual females provisioning pups. Females travelled an average of 118 ± 50 km from their colony during foraging trips that lasted 7.3 ± 3.4 days. Comparison of two methods for calculating foraging intensity (first-passage time and first-passage time modified to include diving behaviour) determined that, due to extended surface intervals where individuals did not travel, inclusion of diving behaviour into foraging analyses was important for this species. Foraging intensity ‘hot spots’ were found to exist in a mosaic of patches within the Bass Basin, primarily to the south-west of the colony. However, the composition of benthic habitat being targeted remains unclear. When increasing their foraging intensity, individuals tended to perform dives around 148 s or greater, with descent/ascent rates of approximately 1.9 m•s^-1 or greater and reduced postdive durations. This suggests individuals were maximising their time within the benthic foraging zone. Furthermore, individuals increased tortuosity and decreased travel speeds while at the surface to maximise their time within a foraging location. These results suggest Australian fur seals will modify both surface movements and diving behaviour to maximise their time within a foraging patch.     

The comparative biology of diving in two genera of European Dytiscidae (Coleoptera)

Surfacing behaviour is fundamental in the ecology of aquatic air-breathing organisms; however, it is only in vertebrates that the evolutionary ecology of diving has been well characterized. Here, we explore the diving behaviour of dytiscid beetles, a key group of surface-exchanging freshwater invertebrates, by comparing the dive responses of 25 taxa (Deronectes and Ilybius spp.) acclimated at two temperatures. The allometric slopes of dive responses in these dytiscids appear similar to those of vertebrate ectotherms, supporting the notion that metabolic mode shapes the evolution of diving performance. In both genera, beetles spend more time submerged than on the surface, and surface time does not vary with the temperature of acclimation. However, presumably in order to meet increased oxygen demand at higher temperatures, Deronectes species increase surfacing frequency, whereas Ilybius species decrease dive time, an example of 'multiple solutions.' Finally, widespread northern species appear to possess higher diving performances than their geographically restricted southern relatives, something which may have contributed to their range expansion ability.     

To what extent is the foraging behaviour of aquatic birds constrained by their physiology?

Aquatic birds have access to limited amounts of usable oxygen when they forage (dive) underwater, so the major physiological constraint to their behaviour is the need to periodically visit the water surface to replenish these stores and remove accumulated carbon dioxide. The size of the oxygen stores and the rate at which they are used (V dot o2) or carbon dioxide accumulates are the ultimate determinants of the duration that aquatic birds can remain feeding underwater. However, the assumption that the decision to terminate a dive is governed solely by the level of the respiratory stores is not always valid. Quantification of an optimal diving model for tufted ducks (Aythya fuligula) shows that while they dive efficiently by spending a minimum amount of time on the surface to replenish the oxygen used during a dive, they dive with nearly full oxygen stores and surface well before these stores are exhausted. The rates of carbon dioxide production during dives and removal during surface intervals are likely to be at least as important a constraint as oxygen; thus, further developments of optimal diving models should account for their effects. In the field, diving birds will adapt to changing environmental conditions and often maximise the time spent submerged during diving bouts. However, other factors influence the diving depths and durations of aquatic birds, and in some circumstances they are unable to forage sufficiently well to provide food for their offspring. The latest developments in telemetry have demonstrated how diving birds can make physiological decisions based on complex environmental factors. Diving penguins can control their inhaled air volume to match the expected depth, likely prey encounter rate, and buoyancy challenges of the following dive.     

A phylogenetic analysis of the allometry of diving

The oxygen store/usage hypothesis suggests that larger animals are able to dive for longer and hence deeper because oxygen storage scales isometrically with body mass, whereas oxygen usage scales allometrically with an exponent <1 (typically 0.67-0.75). Previous tests of the allometry of diving tend to reject this hypothesis, but they are based on restricted data sets or invalid statistical analyses (which assume that every species provides independent information). Here we apply information-theoretic statistical methods that are phylogenetically informed to a large data set on diving variables for birds and mammals to describe the allometry of diving. Body mass is strongly related to all dive variables except dive:pause ratio. We demonstrate that many diving variables covary strongly with body mass and that they have allometric exponents close to 0.33. Thus, our results fail to falsify the oxygen store/usage hypothesis. The allometric relationships for most diving variables are statistically indistinguishable for birds and mammals, but birds tend to dive deeper than mammals of equivalent mass. The allometric relationships for all diving variables except mean dive duration are also statistically indistinguishable for all major taxonomic groups of divers within birds and mammals, with the exception of the procellariiforms, which, strictly speaking, are not true divers.     

Seasonal and annual variation in the diving behaviour of Hutton's shearwater (Puffinus huttoni)

ABSTRACT

With the development and implementation of tracking technology, we are now able to monitor the foraging behaviour of seabirds while at sea. Time-Depth Recorders (TDRs) were fitted to Hutton's shearwaters (Puffinus huttoni), an endangered endemic New Zealand species, to measure how diving behaviour varies over the breeding cycle. Hutton's shearwaters (～350?g) dive up to 339 times per day (average 68.8) at depths to 35?m (average 5.6?m), and for periods up to 60?s (average 19.2?s). Incubating birds dived deeper than birds feeding chicks, and a significant difference in diving depth and dive duration were detected at different times of the day. Neither dive frequency nor dive duration differed significantly between years, but there was some annual variation in dive depths. The temporal variation we observed in the diving behaviour of Hutton's shearwaters suggests they are likely to exploit different types of pelagic prey at different stages in their breeding cycle. With on-going changes in the marine environment, monitoring changes in feeding behaviour using TDRs may provide a way to assess environmental change and improve the conservation of this species.     

Summer diet of seabirds feeding in sea-ice-covered waters near Svalbard

Summary We describe the summer diets of four seabird species. Kittiwake (Rissa tridactyla), Little Auk (Alle alle), Black Guillemot (Cepphus grylle) and Brünnich's Guillemot (Uria lomvia) collected in sea-ice-covered waters near Svalbard. Birds collected in an area filled with young sea-ice, within the seasonal sea-ice zone, were compared with birds collected from the perennial sea-ice zone dominated by multiyear ice. Pelagic Crustacea and fish dominated the diet of birds feeding in young ice, while sympagic Crustacea and fish were most important in the diet of birds feeding in multiyear ice. Boreogadus saida was the most important fish food item. B. Saida was present in the ice in both areas, while sympagic Crustacea were lacking in the area filled with young ice. Important food items in young ice were B. saida (Black Guillemots and Kittiwakes), Cajanus sp. (Little Auks) and Pandalus borealis (Brünnich's Guillemot). B. saida (Black Guillemots, Kittiwakes, Brünnich's Guillemots), Gammarus wilkitzkii (Brünnich's Guillemot, Black Guillemot) and Apherusa glacialis (Little Auk) were most important in multiyear ice. In general, Black Guillemots and Kittiwakes fed on fish, whereas Brünnich's Guillemots fed on the larger, and Little Auks on the smaller, Crustacea. The importance of sympagic species in the diet of seabirds is thought to be closely related to the age and history of the ice in the feeding area.     

Winter diets of four seabird species in the Barents Sea after a crash in the capelin stock

Summary I describe the winter diets (early March) of four seabird species, black-legged kittiwake (Rissa tridactyla), northern fulmar (Fulmarus glacialis), glaucous gull (Larus hyperboreus) and Brüinnich's guillemot (Uria lomvia) collected in the south eastern Barents Sea, in open water approximately 70 km from the ice edge. All species preyed heavily on commercial fish species such as cod (Gadus morrhua), polar cod (Boreogadus saida) and redfish (Sebastes marinus/S. mentella). The median total length of fish eaten ranged from 51 mm in fulmars to 88 mm in Brünnich's guillemots and differed significantly among all species pairs except kittiwake and glaucous gull. Although the size of fish eaten differed among the four bird species they all fed upon much the same age categories of fish. Cod and redfish eaten were almost exclusively one year old, whereas polar cod was 1–4 years old. Other important food items were crustaceans (B unnich's guillemots), and squid Gonatus sp. (fulmars); the glaucous gull also preyed on other birds. Body weights and amounts of stored fat suggest that individuals of all species except Brüinnich's guillemots were in good physical condition. The diets described here differed substantially from those of birds caught mainly during the prelaying season near the colonies in this area. Some of these differences may be attributed to the very low density of capelin (Mallotus villosus) when this study was conducted.     

Long-term monitoring of leatherback turtle diving behaviour during oceanic movements

The diving behaviour of four leatherback turtles (Dermochelys coriacea) was recorded for periods of 0.5-8.1 months during their postnesting movements in the Indian and Atlantic Oceans, when they covered 1569-18,994 km. Dive data were obtained using satellite-linked transmitters which also provided information on the dive depths and profiles of the turtles. Turtles mainly dove to depths < 200 m, with maximum dive durations under 30-40 min and exhibited diel variations in their diving activity for most part of the routes, with dives being usually longer at night. Diurnal dives were in general quite short, but cases of very deep (> 900 m) and prolonged (> 70 min) dives were however recorded only during daytime. The three turtles that were tracked for the longest time showed a marked change in behaviour during the tracking, decreasing their dive durations and ceasing to dive deeply. Moreover, diel variations disappeared, with nocturnal dives becoming short and numerous. This change in turtle diving activity appeared to be related to water temperature, suggesting an influence of seasonal prey availability on their diving behaviour. The turtle diving activity was independent on the shape of their routes, with no changes between linear movements in the core of main currents or looping segments in presence of oceanic eddies.     

Testing optimal foraging theory in a penguin–krill system

Food is heterogeneously distributed in nature, and understanding how animals search for and exploit food patches is a fundamental challenge in ecology. The classic marginal value theorem (MVT) formulates optimal patch residence time in response to patch quality. The MVT was generally proved in controlled animal experiments; however, owing to the technical difficulties in recording foraging behaviour in the wild, it has been inadequately examined in natural predator–prey systems, especially those in the three-dimensional marine environment. Using animal-borne accelerometers and video cameras, we collected a rare dataset in which the behaviour of a marine predator (penguin) was recorded simultaneously with the capture timings of mobile, patchily distributed prey (krill). We provide qualitative support for the MVT by showing that (i) krill capture rate diminished with time in each dive, as assumed in the MVT, and (ii) dive duration (or patch residence time, controlled for dive depth) increased with short-term, dive-scale krill capture rate, but decreased with long-term, bout-scale krill capture rate, as predicted from the MVT. Our results demonstrate that a single environmental factor (i.e. patch quality) can have opposite effects on animal behaviour depending on the time scale, emphasizing the importance of multi-scale approaches in understanding complex foraging strategies.     

Optimal diving behaviour for foraging in relation to body size

Overall, large animals dive longer and deeper than small animals; however, after the difference in body size is taken into account, smaller divers often tend to make relatively longer dives. Neither physiological nor theoretical explanations have been provided for this paradox. This paper develops an optimal foraging diving model to demonstrate the effect of body size on diving behaviour, and discusses optimal diving behaviour in relation to body size. The general features of the results are: (1) smaller divers should rely more heavily on anaerobic respiration, (2) larger divers should not always make longer dives than smaller divers, and (3) an optimal body size exists for each diving depth. These results explain the relatively greater diving ability observed in smaller divers, and suggest that if the vertical distribution of prey in the water column is patchy, there is opportunity for a population of diving animals to occupy habitat niches related to body size.