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.     

The influence of subsurface thermal structure on the diving behavior of northern fur seals (<Emphasis Type="Italic">Callorhinus ursinus</Emphasis>) during the breeding season

In the heterogeneous marine environment, predators can increase foraging success by targeting physical oceanographic features, which often aggregate prey. For northern fur seals (Callorhinus ursinus), two prevalent oceanographic features characterize foraging areas during summer in the Bering Sea: a stable thermocline and a subsurface “cold pool”. The objective of this study was to examine the influence of these features on foraging behavior by equipping fur seals from St. Paul Island (Alaska, USA) with time-depth recorders that also measured water temperature. Foraging bout variables (e.g., mean dive depth and percent time diving in a bout) were compared with respect to subsurface thermal characteristics (thermocline presence and strength and cold pool presence). Over 74% of bouts occurred in association with strong thermoclines (temperature change > 5°C). Few differences were found for dive behavior in relation to the presence of a thermocline and the cold pool, but for epipelagic bouts, a strong thermocline resulted in increased bottom times, number of dive wiggles, and percent time diving when compared to moderate thermoclines. There was also a positive relationship between mean dive depth and thermocline depth. The combination of increasing foraging effort in areas with strong thermoclines and diving to depths closely related to the thermocline indicates this feature is important foraging habitat for northern fur seals and may act to concentrate prey and increase foraging success. By recognizing the environmental features northern fur seals use to find prey, managers will be better equipped to identify and protect foraging habitat that is important to northern fur seals, and possibly other marine predators in the Bering Sea.     

Identification of distinct movement patterns in Pacific leatherback turtle populations influenced by ocean conditions

Interactions with fisheries are believed to be a major cause of mortality for adult leatherback turtles (Dermochelys coriacea), which is of particular concern in the Pacific Ocean, where they have been rapidly declining. In order to identify where these interactions are occurring and how they may be reduced, it is essential first to understand the movements and behavior of leatherback turtles. There are two regional nesting populations in the East Pacific (EP) and West Pacific (WP), comprising multiple nesting sites. We synthesized tracking data from the two populations and compared their movement patterns. A switching state-space model was applied to 135 Argos satellite tracks to account for observation error, and to distinguish between migratory and area-restricted search behaviors. The tracking data, from the largest leatherback data set ever assembled, indicated that there was a high degree of spatial segregation between EP and WP leatherbacks. Area-restricted search behavior mainly occurred in the southeast Pacific for the EP leatherbacks, whereas the WP leatherbacks had several different search areas in the California Current, central North Pacific, South China Sea, off eastern Indonesia, and off southeastern Australia. We also extracted remotely sensed oceanographic data and applied a generalized linear mixed model to determine if leatherbacks exhibited different behavior in relation to environmental variables. For the WP population, the probability of area-restricted search behavior was positively correlated with chlorophyll-a concentration. This response was less strong in the EP population, but these turtles had a higher probability of search behavior where there was greater Ekman upwelling, which may increase the transport of nutrients and consequently prey availability. These divergent responses to oceanographic conditions have implications for leatherback vulnerability to fisheries interactions and to the effects of climate change. The occurrence of leatherback turtles within both coastal and pelagic areas means they have a high risk of exposure to many different fisheries, which may be very distant from their nesting sites. The EP leatherbacks have more limited foraging grounds than the WP leatherbacks, which could make them more susceptible to any temperature or prey changes that occur in response to climate change.     

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.     

Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species

Chemotactile cues unintentionally left by animals can play a major role in predator–prey interactions. Specialized predators can use them to find their prey, while prey individuals can assess predation risk. However, little is known to date about the importance of chemotactile cues for generalist predators such as ants. Here, we investigated the response of a generalized predatory ant, Formica polyctena, to cues of two taxonomically distinct prey: a spider (Pisaura mirabilis) and a cricket (Nemobius sylvestris). In analogy, we studied whether crickets and spiders showed antipredator behavior in response to ant cues. When confronted with cues of the two prey species, Formica polyctena workers showed increased residence time and reduced movement speed, which suggests success-motivated searching behavior and thus increased foraging effort. The ants’ response did not differ between cues of the two prey species, coinciding with similar aggression and consumption rates of dead prey. However, the cuticular hydrocarbons, which likely resemble part of the potential cues, differed strongly between the species, with only few methyl-branched alkanes in common. This suggests that ants respond to multiple compounds left by other organisms with prey-search behavior. The two prey species, in turn, showed no detectable antipredator behavior in response to ant cues. Our study shows that ants can detect and respond to chemotactile cues of taxonomically and ecologically distinct prey species, probably to raise their foraging success. Using such chemotactile cues for prey detection may drastically increase their foraging efficiency and thus contribute to the high ecological success of ants.     

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.     

Search behavior of the checker-throated antwren foraging in aerial leaf litter

Summary Checker-throated antwrens (Formicariidae: Myrmotherula fulviventris) live in lowland neotropical forests and forage from dead curled leaves in the understory. Because they search each leaf individually they provide an opportunity to study the use of potential visual cues by an insectivorous bird. Long and highly curled leaves contain the most arthropods and checker-throated antwrens were more successful when foraging at those leaves. Yet, they used leaves at random with respect to these potential cues. Antwrens spent longer searching for arthropods in each highly curled leaf than in less curled leaves. Because of this additional search time, prey capture success per unit foraging time was only slightly greater for highly curled leaves than at the average dead leaf in the aerial leaf litter. Thus, the cues that antwrens could use to locate richer leaves are those features that obscure the prey from avian predators. Unlike other foraging systems, the antwrens appear to have no reliable cues indicating more profitable foraging sites.Address for correspondence     

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.     

Age-related shifts in the diet composition of southern elephant seals expand overall foraging niche

Southern elephant seals are important apex predators in a highly variable and unpredictable marine environment. In the presence of resource limitation, foraging behaviours evolve to reduce intra-specific competition increasing a species’ overall probability of successful foraging. We examined the diet of 141 (aged 1–3 years) juvenile southern elephant seals to test the hypotheses that differences between ages, sexes and seasons in diet structure occur. We described prey species composition for common squid and fish species and the mean size of cephalopod prey items for these age groups. Three cephalopod species dominated the stomach samples, Alluroteuthis antarcticus, Histioteuthis eltaninae and Slosarczykovia circumantarcticus. We found age-related differences in both species composition and size of larger prey species that probably relate to ontogenetic changes in diving ability and haul-out behaviour and prey availability. These changes in foraging behaviour and diet are hypothesised to reduce intra-specific food competition concomitant with the increase in foraging niche of growing juveniles.     

Underwater and above-water search patterns of an Arctic seabird: reduced searching at small spatiotemporal scales

How predators vary search patterns in response to prey predictability is poorly known. For example, marine invertebrates may be predictable but of low energy value, while fish may be of higher energy value but unpredictable at large (pelagic schools) or small (solitary benthics) spatial scales. We investigated the search patterns of the thick-billed murre (Uria lomvia), an Arctic seabird feeding on invertebrates, pelagic fish, or benthic fish. Foraging ranges at the Coats Island colony are generally smaller (<240 min per trip) than at larger colonies, and many birds specialize in foraging tactics and diet. Underwater search times for benthic fish were higher than for pelagic fish or invertebrates while above-water search times for pelagic fish were higher than for benthic fish or invertebrates. There were few stops during trips. Total trip time, flying time, number of flights, and number of dives were intercorrelated and increased with prey energy content, suggesting that longer trips involved fewer prey encounters due to selection of higher-quality, but rarer, prey items. Flight times were not Lévy-distributed and seabirds may have used area-restricted searches. The high degree of specialization, apparent absence of information center effects, and reduced above-water searching times may be linked to the relatively small colony size and the resulting short commuting distances to feeding areas, leading to greater prey predictability. We concluded that prey predictability over various scales affected predator search patterns.     

Predators use environmental cues to discriminate between prey

The cognitive processes of predators play a central role in the evolution of prey characters. Numerous studies have shown that vertebrate predators may learn to associate the characteristics of prey (e.g. color) with the cost or benefit of ingesting them, thus forming preferences and aversions for different kinds of prey. Although the distribution and quality of prey types can differ between environmental contexts, which may make it profitable to attack a prey type in some contexts but not in others, the influence of environmental cues in decisions to attack has rarely been addressed. Recent theory suggests that modification of prey preferences by environmental cues such as microhabitat or temperature may influence the evolution of prey characteristics. Here, we show that the environmental foraging context may determine prey choice in great tits (Parus major) through learned association between the prey phenotype (appearance and palatability) and a contextual background cue. The same individuals were able to learn and maintain two different sets of food preferences and aversions for use in two different environmental contexts (aviaries with red or blue wooden boards), indicating a role for contextual learning in vertebrate foraging behavior.     

Linking movement, diving, and habitat to foraging success in a large marine predator

Establishing where and when predators forage is essential to understanding trophic interactions, yet foraging behavior remains poorly understood in large marine carnivores. We investigated the factors leading to foraging success in gray seals (Halichoerus grypus) in the Northwest Atlantic in the first study to use simultaneous deployments of satellite transmitters, time depth recorders, and stomach-temperature loggers on a free-ranging marine mammal. Thirty-two seals were each fitted with the three types of instrumentation; however, complete records from all three instruments were obtained from only 13 individuals, underscoring the difficulty of such a multi-instrument approach. Our goal was to determine the characteristics of diving, habitat, and movement that predict feeding. We linked diving behavior to foraging success at two temporal scales: trips (days) and bouts (hours) to test models of optimal diving, which indicate that feeding can be predicted by time spent at the bottom of a dive. Using an information-theoretic approach, a Generalized Linear Mixed Model with trip duration and accumulated bottom time per day best explained the number of feeding events per trip, whereas the best predictor of the number of feeding events per bout was accumulated bottom time. We then tested whether characteristics of movement were predictive of feeding. Significant predictors of the number of feeding events per trip were angular variance (i.e., path tortuosity) and distance traveled per day. Finally, we integrated measures of diving, movement, and habitat at four temporal scales to determine overall predictors of feeding. At the 3-h scale, mean bottom time and distance traveled were the most important predictors of feeding frequency, whereas at the 6-h and 24-h time scales, distance traveled alone was most important. Bathymetry was the most significant predictor of feeding at the 12-h interval, with feeding more likely to occur at deeper depths. Our findings indicate that several factors predict feeding in gray seals, but predictor variables differ across temporal scales such that environmental variation becomes important at some scales and not others. Overall, our results illustrate the value of simultaneously recording and integrating multiple types of information to better understand the circumstances leading to foraging success.     

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.     

Predatory behavior ofPhacellophora camtschatica and size-selective predation uponAurelia aurita (Scyphozoa: Cnidaria) in Saanich Inlet,British Columbia

Predation uponAurelia aurita byPhacellophora camtschatica was studied by SCUBA divers in a fjord in British Columbia between July and September 1986. The behavior and size ofP. camtschatica affected their foraging success. Larger predators captured more and larger prey. The size and behavior of the prey also affected the probability of capture. Predators were found at densities which can affect both the size composition and the overall numbers of the prey population.     

Water column use and forage strategies of female southern elephant seals from Marion Island

The at-sea behaviour of marine top predators provides valuable insights into the distribution of prey species and strategies used by predators to exploit patchily distributed resources. We describe the water column usage and dive strategies of female southern elephant seals from Marion Island tracked between 2004 and 2008. Dives representing increases in forage effort were identified using a method that combines dive type analyses and the calculation of relative amounts of time that animals spend in the bottom phases of dives. Results from this analysis indicate that female elephant seals from Marion Island tend to display lower levels of forage effort closer to the island and display intensive opportunistic forage bouts that occur at a minimum distance of approximately 215 km from the island. Females from Marion Island dived deeper and for longer periods of time, compared to females from other populations. Most animals displayed positive diel vertical migration, evidently foraging pelagically on vertically migrating prey. A few animals displayed periods of reverse (negative) diel vertical migration, however, diving to deeper depths at night, compared to daytime. This behaviour is difficult to explain and prey species targeted during such periods unknown. Our results illustrate plasticity in foraging behaviour of southern elephant seals, as well as inter-population differences in forage strategies.     

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.     

Size and seasonal influences on the foraging range of female grey seals in the northeast Atlantic

Evidence of segregation in foraging habitat has been demonstrated in some top marine predators, including cetaceans, pinnipeds and seabirds. However, most data are not adequate to assess differences relating to body size or seasonal influences. This has implications for quantitative modelling of population-level predator–prey interactions and ecosystem structure. We examined potential influence of body size and ‘fatness’ on the foraging trip characteristics of a top marine predator, the Atlantic grey seal (Halichoerus grypus), in southwest Ireland within the framework of optimal foraging theory to examine how female grey seals foraging behaviour varied with size, and across the period between moult and breeding. Larger seals undertook trips of greater duration and travelled further from haul-out sites than smaller seals. However, body fat was negatively associated with trip duration and extent. Seals spent more time at sea during the summer, but trips were shorter in extent, suggesting more localized foraging during this season.     

A predator’s body coloration enhances its foraging profitability by day and night

Few predators forage by both day and night. It remains unknown, however, how the costs and benefits of foraging or signaling are partitioned in animals that forage at all times. The orb-web spider Cyrtophora moluccensis is brightly colored and forages by day and night. We determined the benefits reaped when it forages by both day and night by estimating the biomass of prey caught in their webs. Additionally, we quantified whether the spider’s presence influences the number of prey caught by day and night and whether its colorful body is visible to diurnal and/or nocturnal insects using diurnal and nocturnal insect vision models. We found that approximately five times the biomass of prey was caught in C. moluccensis’ webs by night than by day. Hemipterans, hymenopterans, and dipterans were predominantly caught by day, while lepidopterans (moths) were predominately caught by night. Accordingly, we concluded that foraging by night is more profitable than foraging by day. We predicted that other benefits, for example, energetic advantages or enhanced fecundity, may promote its daytime activity. Foraging success was greater by day and night when the spider was present in the web than when the spider was absent. We also found that parts of the spider’s body were conspicuous to diurnal and nocturnal insects, possibly through different visual channels. The colorful body of C. moluccensis, accordingly, appears to influence its foraging success by attracting prey during both the day and night.     

Behavioral resource depression and decaying perceived risk of predation in two species of coexisting gerbils

Summary Behavioral resource depression occurs when the behavior of prey individuals changes in response to the presence of a predator, resulting in a reduction of the encounter rate of the predator with its prey. Here I present experimental evidence on the response of two species of gerbils (Gerbillus allenbyi and G. pyramidum) to the presence of barn owls. I conducted the experiments in a large aviary. Both gerbils responded to the presence of barn owl predators by foraging in fewer resource patches (seed trays) and by quitting foraged resource patches at a higher resource harvest rate (giving-up density of resource; GUD). This reduced the amount of time gerbils were exposed to owl predation, and hence the encounter rate of owls with gerbils, i.e., behavioral resource depression. Thus, the presence of owls imposes a foraging cost on gerbils due to risk of predation, and also on the owls themselves due to resource depression. I then examined how resource depression relaxed over time following exposure to owls. In the days following an encounter with the predator, the reduction in foraging activity for both gerbil species eased. Increasing numbers of trays were foraged each day, and GUDs in seed trays declined. The two gerbils differed in their rate of recovery, with G. pyramidum returning to prepredator levels of foraging after 1 or 2 nights and G. allenbyi taking 5 nights or longer. Interspecific differences in recovery rates may be based on differences between the species in vulnerability to predation and/or ability to detect the presence of predators. The differences in recovery rates may be due to optimal memory windows or decay rates, where differences between species are based on risk of predation or on how perceived risk changes with time since a predator was last encountered. Finally, differences between or among competitors in recovery from resource depression may provide foraging opportunities in time for the species which recover most quickly and may have implications for species coexistence.     

Costs and benefits of pocket gopher foraging: linking behavior and physiology

Animals can attain fitness benefits by maintaining a positive net energy balance, including costs of movement during resource acquisition and the profits from foraging. Subterranean rodent burrowing provides an excellent system in which to examine the effects of movement costs on foraging behavior because it is energetically expensive to excavate burrows. We used an individual-based modeling approach to study pocket gopher foraging and its relationship to digging cost, food abundance, and food distribution. We used a unique combination of an individual-based foraging-behavior model and an energetic model to assess survival, body mass dynamics, and burrow configurations. Our model revealed that even the extreme cost of digging is not as costly as it appears when compared to metabolic costs. Concentrating digging in the area where food was found, or area-restricted search (ARS), was the most energetically efficient digging strategy compared to a random strategy. Field data show that natural burrow configurations were more closely approximated by the animals we modeled using ARS compared to random diggers. By using behavior and simple physiological principles in our model, we were able to observe realistic body mass dynamics and recreate natural movement patterns.