Do activity costs determine foraging tactics for an arctic seabird?

How energy costs affect foraging decisions is poorly understood for marine animals. To provide data relevant to this topic, we examined the relationship between activity levels and foraging behavior by attaching activity recorders to 29 chick-rearing wing-propelled diving birds (thick-billed murres, Uria lomvia) in 1999–2000. We connected the activity during the final dive bout with the prey item we observed being fed to the chicks. After accounting for changes in activity level with depth, activity was highest during the final dive of a dive bout, reflecting maneuvring during prey capture. Pelagic prey items, especially invertebrates (amphipods), were associated with higher depth-corrected activity, leading to shorter dives for a given depth (presumably due to higher oxygen consumption rates) and, thus, shorter search times (lower bottom time for a given depth). Pelagic prey items were likely captured during active pursuit, with the birds actively seeking and pursuing schooling mid-water prey. In contrast, benthic prey involved low activity and extended search times, suggesting that the birds slowly glided along the bottom in search for prey hidden in the sediments or rocks. We concluded that activity levels are important in determining the foraging tactics of marine predators. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Going deep: common murres dive into frigid water for aggregated,persistent and slow-moving capelin

Owing to the necessity of delivering food to offspring at colonies, breeding seabirds are highly constrained in their foraging options. To minimize constraints imposed by central-place foraging and to optimize foraging behavior, many species exhibit flexible foraging tactics. Here we document the behavioral flexibility of pursuit-diving common murres Uria aalge when foraging on female capelin Mallotus villosus in the northwest Atlantic. Quite unexpectedly, being visual foragers, we found that common murres dived throughout the day and night. Twenty-one percent of recorded dives (n = 272 of 1,308 dives) were deep (≥50 m; maximum depth = 152 m, maximum duration = 212 s), bringing murres into sub-0°C water in the Cold Intermediate Layer (CIL; 40–180 m) of the Labrador Current. Deep dives occurred almost exclusively during the day when murres would have encountered spatially predictable aggregations of capelin between 100 and 150 m in the water column. Temperatures within the CIL shaped trophic interactions and involved trade-offs for both predators and prey. Sub-0°C temperatures limit a fish’s ability to escape from endothermic predators by reducing burst/escape speeds and also lengthening the time needed to recover from burst-type activity. Thus, while deep diving may be energetically costly, it likely increases certainty of prey capture. Decreased murre foraging efficiency at night (indicated by an increase in the number of dives per bout) reflects both lower light conditions and changing prey behavior, as capelin migrate to warmer surface waters at night where their potential to escape from avian predators could increase.     

A Bayesian hierarchical model of Antarctic fur seal foraging and pup growth related to sea ice and prey abundance

We created a Bayesian hierarchical model (BHM) to investigate ecosystem relationships between the physical ecosystem (sea ice extent), a prey measure (krill density), predator behaviors (diving and foraging effort of female Antarctic fur seals, Arctocephalus gazella, with pups) and predator characteristics (mass of maternal fur seals and pups). We collected data on Antarctic fur seals from 1987/1988 to 1994/1995 at Seal Island, Antarctica. The BHM allowed us to link together predators and prey into a model that uses all the data efficiently and accounts for major sources of uncertainty. Based on the literature, we made hypotheses about the relationships in the model, which we compared with the model outcome after fitting the BHM. For each BHM parameter, we calculated the mean of the posterior density and the 95% credible interval. Our model confirmed others' findings that increased sea ice was related to increased krill density. Higher krill density led to reduced dive intensity of maternal fur seals, as measured by dive depth and duration, and to less time spent foraging by maternal fur seals. Heavier maternal fur seals and lower maternal foraging effort resulted in heavier pups at 22 d. No relationship was found between krill density and maternal mass, or between maternal mass and foraging effort on pup growth rates between 22 and 85 days of age. Maternal mass may have reflected environmental conditions prior to the pup provisioning season, rather than summer prey densities. Maternal mass and foraging effort were not related to pup growth rates between 22 and 85 d, possibly indicating that food was not limiting, food sources other than krill were being used, or differences occurred before pups reached age 22 d.     

Multi-scale foraging variability in Northern gannet (Morus bassanus) fuels potential foraging plasticity

The survival of marine predators depends on behavioural plasticity to cope with changes in prey distribution. Variability in behaviour might predict plasticity and is easier to assess than plasticity. Using miniaturized GPS loggers over several breeding seasons in two Norwegian Northern gannet (Morus bassanus) colonies, we investigated if and how the variability within and between individuals, but also between colonies and years, affected foraging strategies. Results revealed strong individual variability (foraging trip durations, foraging effort and different foraging areas). Individuals from both colonies showed preferred commuting routes, flight bearings and feeding hotspots. Individuals from the largest colony used larger and more foraging areas than individuals from the small colony. Feeding hotspots and foraging ranges varied amongst years in the largest colony only. Our study demonstrated that gannets show flexibility by changing prey fields that are driven by shifting oceanographic conditions.     

Behavioural inertia places a top marine predator at risk from environmental change in the Benguela upwelling system

In variable environments, organisms are bound to track environmental changes if they are to survive. Most marine mammals and seabirds are colonial, central-place foragers with long-term breeding-site fidelity. When confronted with environmental change, such species are potentially constrained in their ability to respond to these changes. For example, if environmental conditions deteriorate within their limited foraging range, long-lived species favour adult survival and abandon their current breeding effort, which ultimately influences population dynamics. Should poor conditions persist over several seasons, breeding-site fidelity may force animals to continue breeding in low-quality habitats instead of emigrating towards more profitable grounds. We assessed the behavioural response of a site-faithful central-place forager, the Cape gannet Morus capensis, endemic to the Benguela upwelling system, to a rapid shift in the distribution and abundance of its preferred prey, small pelagic shoaling fish. We studied the distribution and the abundance of prey species, and the diet, foraging distribution, foraging effort, energy requirements, and breeding success of gannets at Malgas Island (South Africa) over four consecutive breeding seasons. Facing a rapid depletion of preferred food within their foraging range, Cape gannets initially increased their foraging effort in search of their natural prey. However, as pelagic fish became progressively scarcer, breeding birds resorted to scavenging readily available discards from a nearby demersal fishery. Their chicks cannot survive on such a diet, and during our 4-year study, numbers of breeding birds at the colony decreased by 40% and breeding success of the remaining birds was very low. Such behavioural inflexibility caused numbers of Cape gannets breeding in Namibia to crash by 95% following over-fishing of pelagic fish in the 1970s. In the context of rapid environmental changes, breeding-site fidelity of long-lived species may increase the risk of local or even global extinction, rendering these species particularly vulnerable to global change.     

An energy–distance trade-off in a central-place forager,the Antarctic fur seal (<Emphasis Type="Italic">Arctocephalus gazella</Emphasis>)

We tested the prediction that lactating fur seals (Arctocephalus gazella) at South Georgia will take prey of greater energy density with increasing distance of foraging from the colony. The study investigated the differences in diet of fur seals foraging within two regions, one near the breeding colony and the other at greater distance. Diet varied significantly in relation to foraging location. Dietary items of low quality were eaten in both regions but more food items with a high-energy content appeared in the diet of seals travelling to distant oceanic waters. We conclude that there is likely to be a trade-off between energy gain and distance travelled which enables female fur seals to maintain a relatively constant rate of energy delivery to their offspring irrespective of the distance travelled to find food.     

Linking marine predator diving behavior to local prey fields in contrasting habitats in a subarctic glacial fjord

Foraging theory predicts that animals will adjust their foraging behavior in order to maximize net energy intake and that trade-offs may exist that can influence their behavior. Although substantial advances have been made with respect to the foraging ecology of large marine predators, there is still a limited understanding of how predators respond to temporal and spatial variability in prey resources, primarily due to a lack of empirical studies that quantify foraging and diving behavior concurrently with characteristics of prey fields. Such information is important because changes in prey availability can influence the foraging success and ultimately fitness of marine predators. We assessed the diving behavior of juvenile female harbor seals (Phoca vitulina richardii) and prey fields near glacial ice and terrestrial haulout sites in Glacier Bay (58°40′N, ?136°05′W), Alaska. Harbor seals captured at glacial ice sites dived deeper, had longer dive durations, lower percent bottom time, and generally traveled further to forage. The increased diving effort for seals from the glacial ice site corresponded to lower prey densities and prey at deeper depths at the glacial ice site. In contrast, seals captured at terrestrial sites dived shallower, had shorter dive durations, higher percent bottom time, and traveled shorter distances to access foraging areas with much higher prey densities at shallower depths. The increased diving effort for seals from glacial ice sites suggests that the lower relative availability of prey may be offset by other factors, such as the stability of the glacial ice as a resting platform and as a refuge from predation. We provide evidence of differences in prey accessibility for seals associated with glacial ice and terrestrial habitats and suggest that seals may balance trade-offs between the costs and benefits of using these habitats.     

Costs and benefits of territorial defense in wild golden lion tamarins,Leontopithecus rosalia

Summary The costs and benefits of territorial defense were examined in a group of five wild golden lion tamarins, Leontopithecus rosalia, at Poco d'Antas Biological reserve, Rio de Janeiro, Brazil. I examined the effects of both interference and exploitative competition between groups of tamarins by comparing their use of space, time budgets and foraging success in different contexts of intergroup interactions and in quadrats shared and not shared by other groups. Tamarins spent more time moving and vocalizing, and less time feeding, foraging, and resting during intergroup encounters than in non-encounter contexts. Irrespective of intergroup distance, the group spent more time in overlapping areas of the range periphery than expected on the basis of quadrat availability. In those areas, however, foraging success per unit of foraging effort was lower than in exclusive areas of the range center. This suggests that access to high payoff central areas depended on costly defense (by both interference and exploitation) of the range periphery. Time and energy invested by the resident group in territorial defense (1) increased the availability of food in the range center, and (2) minimized food loss to neighboring groups in the range periphery. These benefits are likely to justify the costs of defense for an animal which depends on easily-depletable food supplies, such as prey in microhabitats and small concentrations of fruits and nectar.     

Extrinsic and intrinsic determinants of winter foraging and breeding phenology in a temperate seabird

In temperate regions, winter presents animals with a number of challenges including depressed food abundance, increased daily energy requirements, higher frequency of extreme weather events and shortened day length. Overcoming these constraints is critical for overwintering survival and scheduling of future breeding of long-lived species and is likely to be state dependent, associated with intrinsic abilities such as food acquisition rates. We examined the relationship between environmental and intrinsic factors on overwintering foraging and subsequent breeding phenology of the European shag Phalacrocorax aristotelis, a diurnal marine predator. We tested a range of hypotheses relating to overwintering foraging time and location. We found that individuals greatly increased their foraging time in winter to a peak of more than 90% of available daylight at the winter solstice. The seasonal patterns of foraging time appear to be driven by a combination of light levels and weather conditions and may be linked to the availability of the shag's principal prey, the lesser sandeel Ammodytes marinus. There was no evidence that shags dispersed south in winter to increase potential foraging time. Foraging time decreased after the winter solstice and, crucially, was correlated with subsequent breeding phenology, such that individuals that spent less time foraging in February bred earlier. The relationship was much stronger in females than males, in line with their more direct control of timing of breeding. Our results demonstrate that pre-breeding intrinsic foraging ability is critical in determining breeding phenology.     

Prey ecology and behaviour affect foraging strategies in the Great Cormorant

The fine link between a particular dive pattern and a specific prey item represents a challenging task in the analysis of marine predator–prey relationships. There is growing evidence that prey type affects diving seabirds’ foraging strategies, dive shapes and underwater activity costs. This study investigates whether a generalist diver, the Great Cormorant Phalacrocorax carbo, modifies the time budget allocated to prey-capture behaviour and breathing strategies (reactive vs. anticipatory) with respect to the prey type (pelagic vs. benthic). Video recordings of 91 Great Cormorants show how the ecology and behaviour of their main prey, Mullets (Mugilidae) and Flounders Platichthys flesus, affect dive/surface durations and the diving pattern. The demersal habit and the low mobility of Flounders leads to an easy access to prey with an anticipatory strategy. Moreover, the patchy distribution of this fish species increases prey-capture rates. Conversely, Mullets exploit the whole water column and are highly mobile, and this is reflected in the need of performing two sequential dives to capture a prey, both longer and likely more expensive, with a consequent switch of strategy from reactive in the searching phase to anticipatory breathing during prey-capture events. This study provides evidence that a generalist diver may switch between different foraging strategies, and it shows how each of them may be optimal under particular ecological conditions. These constraints influence the dynamics that operate within the marine food chains and have relevant implications in managing lagoon areas, including fish ponds.     

Predatory feeding of two marine mysids

Predatory feeding of the marine mysids Mysidopsis bigelowi and Neomysis americana on several species of co-occurring copepods was examined in laboratory experiments. M. bigelowi exhibited a curvilinear functional response; there was a negative logarithmic relationship between prey density and clearance rates. N. americana also exhibited higher clearance rates at lower prey densities. Increased clearance rates at lower prey densities were probably due to increased swimming speed or reaction distance as hunger increased. This response occurred only when mysids could visually locate prey; in complete darkness clearance rates were significantly lower and independent of prey density. Feeding rates on different prey species were only partially dependent on prey size; prey movement patterns and escape behavior also strongly affected feeding rates. M. bigelowi showed active prey selection when offered a choice of different prey species. Estimates of predation rates of estuarine mysid populations indicate that they could have a significant effect on co-occurring copepod populations.     

Experimental test of the effects of a non-native invasive species on a wintering shorebird

The abundance of nearly one-quarter of the world's shorebird species is declining. At the same time, the number of non-native species in coastal ecosystems is increasing rapidly. In some cases, non-native species may affect negatively the abundance and diversity of shorebird prey species. We conducted an experimental study of the effects of the introduced European green crab (Carcinus maenas) on prey consumption by wintering Dunlin (Calidris alpina) in a central California estuary. We placed green crabs and Dunlin sequentially in field enclosures and measured changes in density of benthic invertebrate prey (e.g. polychaetes and small clams), Dunlin biomass, and gut contents of both Dunlin and crabs and observed foraging behavior of Dunlin. Green crabs significantly affected Dunlin foraging success through both direct and indirect multitrophic linkages. In enclosures with high densities of green crabs, crab foraging reduced the availability of polychaetes, and Dunlin consumed significantly fewer polychaetes compared with Dunlin in enclosures without crabs. High densities of green crabs were also associated with increased availability of small clams. Dunlin consumed significantly more small clams compared with Dunlin in enclosures without crabs. In our literature survey of studies of effects of non-native invasive species on shorebirds, we found three prior experiments that addressed the effect of non-native invasive species on shorebirds. Results of two of these studies showed positive direct effects of non-native invertebrates on shorebirds, 1 showed negative direct effects of a non-native plant on shorebirds through habitat conversion, and none showed indirect effects of non-native invertebrates. We suggest future management of shorebirds explicitly examine how non-native marine species, particularly invertebrates, directly and indirectly affect shorebirds.     

Forager specialization and the control of nest repair in Polybia occidentalis Olivier (Hymenoptera : Vespidae)

We measured patterns of individual forager specialization and colony-wide rates of material input during periods of response to experimental nest damage and during control periods in three colonies of the tropical social wasp Polybia occidentalis.

Foraging impact on zooplankton by age-0 walleye pollock (<Emphasis Type="Italic">Theragra chalcogramma</Emphasis>) around a front in the southeast Bering Sea

The waters around the Pribilof Islands in the southeast Bering Sea are a center of abundance for age-0 walleye pollock (Theragra chalcogramma). Each spring and summer a tidal front is formed around the islands separating a well-mixed inshore habitat from a stratified offshore habitat. The objective of this study was to assess the foraging impact on zooplankton by age-0 pollock in the vicinity of this frontal structure. A bioenergetic model was used to estimate age-0 pollock food consumption from field estimates of water temperature, age-0 pollock density, diet and growth. Sampling of field variables took place over three hydrographic habitats along an inshore–offshore transect located north of the islands. The bioenergetics analysis was applied for a 2-week period during the late summer of four consecutive years, 1994–1997. Model results of age-0 pollock food consumption indicated variable levels of food depletion, changing with prey type, year and habitat. The foraging impact of age-0 pollock on copepods and euphausiids (most common prey) ranged from about 3% to 77% of the biomass available at the start of the simulation. Copepod depletion was typically greater than euphausiid depletion. Consequently, juvenile pollock <60 mm in standard length were more likely to experience food limitation due to the greater proportion of copepods in their diet. We present evidence of severe foraging impact during 1996, when one of the primary prey items of juvenile pollock (i.e. large copepods) was scarcely represented both in their diet and in the water column. In all years, most instances of prey depletion were found at the inshore and front habitats; age-0 pollock densities were too low relative to their prey to severely impact the offshore zooplankton populations. We discuss these results with respect to modeling assumptions and in the context of previously acquired knowledge of fish behavior around frontal regions.Communicated by T. Ikeda, Hakodate     

Risk-aversion,relative abundance of resources and foraging preference

Summary Foraging theory depicts dietary choice as a function of prey quality and absolute abundance. Ecological processes, however, can depend on the way foragers respond to the relative abundances of available prey types; several models for frequency-dependent foraging adequately describe these responses. Our laboratory experiments with white-throated sparrows investigated preferential choice of two food rewards as we manipulated both reward quality and relative abundance. In any single experiment the two rewards provided the same mean food quantity, but the variances differed. Average energy budgets predicted risk-aversion, so that foraging preference should decrease as reward variance increases. We presented each two-reward pairing at availability ratios of 1:2, 1:1, and 2:1 for three consecutive days. By the third day risk-aversion exceeded preference for reward variance significantly. When relative abundances of the low and high variance rewards were not equal, the birds tended to prefer the rare over the common reward. This response began before the birds had thoroughly sampled the reward distributions. Preference for rarity apparently constrained the birds' economic response to reward variance levels.     

How the mountain chickadee procures more food in less time for its nestlings

Summary Parent mountain chickadees (Parus gambeli) visit the same foraging location on consecutive flights more frequently than expected by chance. This pattern of repetitive return to a foraging location does not increase the frequency of capturing the same prey on consecutive flights. The quantity of prey captured on a visit also does not change significantly with repeated visits to a foraging location. Foraging time, however, is significantly shorter during repeated visits to a foraging location. Foraging time is therefore a major determinant of whether a run of consecutive flights to a location occurs. Decreased foraging time is also a benefit of selecting the same prey type on consecutive flights. Over the course of a day, the prey types returned on the greatest percentage of flights are returned multiply per flight. These prey are usually small and are probably present at high densities in the environment. Large prey size is the second best predictor of frequency of a prey type in the diet. Short foraging time to capture a prey is the third best predictor. Thus prey which can be readily obtained in large numbers, even if they are small prey, are preferentially returned to older nestlings. The mountain chickadee uses information on foraging time to decide when to move to a new foraging location or when to pursue a different type of prey. These decisions should increase the amount of time available for prey gathering.     

Feeding behavior of the sea star Astropecten articulatus (Echinodermata: Asteroidea): an evaluation of energy-efficient foraging in a soft-bottom predator

The energy efficiency of the foraging behavior of Astropecten articulatus (Say) was evaluated in the laboratory. Individuals utilized in the study were collected in the northern Gulf of Mexico from 1990 to 1992. Sea stars presented with equal numbers and weights of low-quality and high-quality prey consistently selected prey of the higher quality. Choice of prey appeared to be mediated by contact chemoreception. Individuals presented with equal weights or equal numbers of different-sized prey models demonstrated a significant preference for smaller prey. Size-selective feeding may be attributable to the ease of manipulation and ingestion of smaller prey, which mazimizes food intake per unit time. In the absence of prey, A. articulatus exhibited a directional pattern of movement. However, as prey were encountered, both the frequency and magnitude of angular deviations in the foraging path increased, resulting in increased foraging in areas of higher prey density. This response to prey availability may increase foraging efficiency by maximizing the rate of prey encounter. Like four other species of the genus Astropecten, A. articulatus exhibited two peaks of activity corresponding with dawn and dusk. Diurnal activities with periods of increased prey availability or periods during which predators are diminished or absent. The sea star A. articulatus exhibits foraging behaviors consistent with the maximization of net energy intake per unit foraging time.     

Inter- and intra-year variation in foraging areas of breeding kittiwakes (Rissa tridactyla)

While seabird conservation efforts have largely focused on protection from threats at the colony (e.g. reducing disturbance and predation), attention is increasingly being given to implementing protection measures for foraging areas at sea. For this to be effective, important foraging areas must be identified. Although numerous studies have examined seabird foraging behaviour, information is still lacking on the variability in area utilisation within and among breeding seasons. GPS devices were attached to adult black-legged kittiwakes breeding at an expanding North Sea colony (55°20′N, 1°32′W) during both incubation and chick-rearing in 2012 and during chick-rearing in 2011, to determine whether foraging areas remained consistent and to identify the oceanographic characteristics of areas used for foraging. The type and size of prey items consumed at different stages of the breeding cycle was also examined. During incubation (April–May 2012), kittiwakes foraged substantially further from the colony and fed on larger sandeels than when feeding chicks, and there was significant inter-annual variation in foraging areas used during the chick-rearing period (June–July 2011 and 2012). Foraging areas were characterised by cooler sea surface temperatures and areas of high chlorophyll a concentration, although association with specific oceanographic features changed within the breeding season and between years. These results emphasise the importance of considering how foraging areas and reliance on specific oceanographic conditions change over time when seeking to identify important marine areas for seabirds.     

Local interactions between predators and prey call into question commonly used functional responses

Commonly used functional response models (Holling’s type I and type II models) assume that the encounter rate of a predator increases linearly with prey density, provided that the predator is searching for prey. In other other words, aN (a is the baseline encounter rate and N is prey density) describes the encounter rate. This study examined whether the models are adequate when predators and prey interact locally by using a spatially explicit individual based model because local interactions affect the spatial distribution of predators and prey, which also affects the encounter rate. Predators were assumed to possess a spatial perception range that influenced their foraging behavior (e.g., if a prey is in the perception range, the predator moves towards the prey). The effect of antipredator behavior by prey was also examined. The results suggest that prey and predator densities as well as handling time affect the baseline rate (i.e., parameter a) as opposed to the common assumption that the parameter is constant. The nature of model deviations depended on both the antipredator behavior and the predators’ perception range. Understanding these deviations is important as they qualitatively affect community dynamics.     

Subhabitat selection by foraging threespine stickleback (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>): previous experience and social conformity

Any mechanism that allows animals to increase their foraging efficiency is likely to be selected for, including the ability to learn to recognise and subsequently discriminate between habitat types based on their profitability. In a series of laboratory studies, we manipulated prey densities across two different experimental subhabitats and demonstrated that threespine stickleback (Gasterosteus aculeatus) can develop foraging preferences for subhabitats that have previously yielded prey. Fish were not recalling the spatial location of prey patches; rather, they were discriminating between subhabitats based on foraging experience there and allocating foraging effort accordingly. Foraging preferences took around 14 days to develop, and once established, they persisted independently of experimental prey density, suggesting that fish were using experience rather than real-time sampling to select foraging grounds. When we presented focal fish with social information cues, we found that they preferentially used local enhancement and current public information cues when they conflicted with previous experience, but that they did not use prior public information. This suggests that in the presence of conspecifics, individuals prioritise social conformity over the use of private information. We discuss our results in the context of optimal foraging and the trade-offs associated with balancing conflicting private and social information.