Fine-scale Foraging Behaviour Research Articles

A taste of space: Remote animal observations and discrete-choice models provide new insights into foraging and density dynamics for a large subarctic herbivore.

Competition for resources and space can drive forage selection of large herbivores from the bite through the landscape scale. Animal behaviour and foraging patterns are also influenced by abiotic and biotic factors. Fine-scale mechanisms of density-dependent foraging at the bite scale are likely consistent with density-dependent behavioural patterns observed at broader scales, but few studies have directly tested this assertion. Here, we tested if space use intensity, a proxy of spatiotemporal density, affects foraging mechanisms at fine spatial scales similarly to density-dependent effects observed at broader scales in caribou. We specifically assessed how behavioural choices are affected by space use intensity and environmental processes using behavioural state and forage selection data from caribou (Rangifer tarandus granti) observed from GPS video-camera collars using a multivariate discrete-choice modelling framework. We found that the probability of eating shrubs increased with increasing caribou space use intensity and cover of Salix spp. shrubs, whereas the probability of eating lichen decreased. Insects also affected fine-scale foraging behaviour by reducing the overall probability of eating. Strong eastward winds mitigated negative effects of insects and resulted in higher probabilities of eating lichen. At last, caribou exhibited foraging functional responses wherein their probability of selecting each food type increased as the availability (% cover) of that food increased. Space use intensity signals of fine-scale foraging were consistent with density-dependent responses observed at larger scales and with recent evidence suggesting declining reproductive rates in the same caribou population. Our results highlight potential risks of overgrazing on sensitive forage species such as lichen. Remote investigation of the functional responses of foraging behaviours provides exciting future applications where spatial models can identify high-quality habitats for conservation.

Predictive model of sperm whale prey capture attempts from time-depth data

BackgroundHigh-resolution sound and movement recording tags offer unprecedented insights into the fine-scale foraging behaviour of cetaceans, especially echolocating odontocetes, enabling the estimation of a series of foraging metrics. However, these tags are expensive, making them inaccessible to most researchers. Time-Depth Recorders (TDRs), which have been widely used to study diving and foraging behaviour of marine mammals, offer a more affordable alternative. Unfortunately, data collected by TDRs are bi-dimensional (time and depth only), so quantifying foraging effort from those data is challenging.MethodsA predictive model of the foraging effort of sperm whales (Physeter macrocephalus) was developed to identify prey capture attempts (PCAs) from time-depth data. Data from high-resolution acoustic and movement recording tags deployed on 12 sperm whales were downsampled to 1 Hz to match the typical TDR sampling resolution and used to predict the number of buzzes (i.e., rapid series of echolocation clicks indicative of PCAs). Generalized linear mixed models were built for dive segments of different durations (30, 60, 180 and 300 s) using multiple dive metrics as potential predictors of PCAs.ResultsAverage depth, variance of depth and variance of vertical velocity were the best predictors of the number of buzzes. Sensitivity analysis showed that models with segments of 180 s had the best overall predictive performance, with a good area under the curve value (0.78 ± 0.05), high sensitivity (0.93 ± 0.06) and high specificity (0.64 ± 0.14). Models using 180 s segments had a small difference between observed and predicted number of buzzes per dive, with a median of 4 buzzes, representing a difference in predicted buzzes of 30%.ConclusionsThese results demonstrate that it is possible to obtain a fine-scale, accurate index of sperm whale PCAs from time-depth data alone. This work helps leveraging the potential of time-depth data for studying the foraging ecology of sperm whales and the possibility of applying this approach to a wide range of echolocating cetaceans. The development of accurate foraging indices from low-cost, easily accessible TDR data would contribute to democratize this type of research, promote long-term studies of various species in several locations, and enable analyses of historical datasets to investigate changes in cetacean foraging activity.

Foraging behaviour of black guillemots at three Norwegian sites during the breeding season

The intensification of coastal development poses potential threats for coastal seabirds, and understanding their habitat use is a key factor to guide conservation and management. In sub-arctic areas, black guillemots (Cepphus grylle) use coastal habitats year-round, which makes them vulnerable to the increasing human activities in these areas. In mainland Norway, one of the species’ strongholds, black guillemots are red-listed after substantial population declines. However, their fine-scale foraging behaviour has received little attention to date. We collected and analysed GPS tracking data from adult black guillemots at three sites located over a latitudinal gradient of 250 km in central/northern Norway. Maximum foraging ranges of 33 km at Sklinna (65°12′N) for incubating birds, and 18 km at both Vega (65°34′N) and Sklinna for chick-rearing birds, are among the longest reported for this species. At all three sites, foraging probability was highest in shallow waters (< 50 m depth) close to the colony and declined with increasing water depth and distance from colony. However, birds from Vega also foraged over deeper waters. Kelp presence was of high importance at Sklinna, but apparently less important at Røst (67°26’N) and Vega. We also found distinct differences in foraging activity across the day and with tidal height among the sites. Inter-site differences in habitat use and foraging activity may be explained by differences in the availability of habitats and suitable prey. Our study highlights the importance of shallow marine areas for black guillemots and shows that habitat use can vary substantially between sites.

Risso's dolphins perform spin dives to target deep-dwelling prey.

Foraging decisions of deep-diving cetaceans can provide fundamental insight into food web dynamics of the deep pelagic ocean. Cetacean optimal foraging entails a tight balance between oxygen-conserving dive strategies and access to deep-dwelling prey of sufficient energetic reward. Risso's dolphins (Grampus griseus) displayed a thus far unknown dive strategy, which we termed the spin dive. Dives started with intense stroking and right-sided lateral rotation. This remarkable behaviour resulted in a rapid descent. By tracking the fine-scale foraging behaviour of seven tagged individuals, matched with prey layer recordings, we tested the hypothesis that spin dives are foraging dives targeting deep-dwelling prey. Hunting depth traced the diel movement of the deep scattering layer, a dense aggregation of prey, that resides deep during the day and near-surface at night. Individuals shifted their foraging strategy from deep spin dives to shallow non-spin dives around dusk. Spin dives were significantly faster, steeper and deeper than non-spin dives, effectively minimizing transit time to bountiful mesopelagic prey, and were focused on periods when the migratory prey might be easier to catch. Hence, whereas Risso's dolphins were mostly shallow, nocturnal foragers, their spin dives enabled extended and rewarding diurnal foraging on deep-dwelling prey.

Fine-scale foraging effort and efficiency of Macaroni penguins is influenced by prey type, patch density and temporal dynamics

Difficulties quantifying in situ prey patch quality have limited our understanding of how marine predators respond to variation within and between patches, and throughout their foraging range. In the present study, animal-borne video, GPS, accelerometer and dive behaviour data loggers were used to investigate the fine-scale foraging behaviour of Macaroni penguins (Eudyptes chrysolophus) in response to prey type, patch density and temporal variation in diving behaviour. Individuals mainly dived during the day and utilised two strategies, targeting different prey types. Subantarctic krill (Euphausia vallentini) were consumed during deep dives, while small soft-bodied fish were captured on shallow dives or during the ascent phase of deep dives. Despite breeding in large colonies individuals seemed to be solitary foragers and did not engage with conspecifics in coordinated behaviour as seen in other group foraging penguin species. This potentially reflects the high abundance and low manoeuvrability of krill. Video data were used to validate prey capture signals in accelerometer data and a Support Vector Machine learning algorithm was developed to identify prey captures that occurred throughout the entire foraging trip. Prey capture rates indicated that Macaroni penguins continued to forage beyond the optimal give up time. However, bout-scale analysis revealed individuals terminated diving behaviour for reasons other than patch quality. These findings indicate that individuals make complex foraging decisions in relation to their proximate environment over multiple spatio-temporal scales.

The dance of the Cape gannet may contain social information on foraging behaviour

Social information percolates through a variety of channels to influence animal decision making, with a notable effect on reproductive and feeding success. Colonial central place foragers can reduce time to locate ephemeral food patches and/or increase foraging rate by following their informed peers, parasitizing direction of returning successful foragers, or being intentionally informed on distant food locations at the colony (e.g. the waggle dance of the honey bee). Ceremonial behaviours may also deliver social foraging information between mates, which can spread inadvertently to neighbours. Here we tested for information display in Cape gannets, Morus capensis, a socially monogamous species, during the elaborate dance ceremony performed each time a partner returns to the nest during the breeding season. We tracked fine-scale foraging behaviour of gannets using bird-borne GPS recorders, and video-recorded their subsequent dance ceremony, which involved up to 14 different displays. As we hypothesized, dance characteristics were associated with foraging trip features. Notably, overall dance duration was negatively linked to foraging trip duration, which was highly positively correlated with foraging range, foraging path length and time spent foraging during the trip. Overall dance duration was also negatively linked with distance to the main foraging grounds. Additionally, the duration of preening behaviour was related to the bearing of the main feeding spot. The latter relationship was supported by a Bayesian model averaging analysis, allowing inferences robust to multiple comparisons. Overall, ceremonial behaviour may provide social foraging information on feeding locations, while evidence for further information transfer to the mate or neighbours was not tested here. Frequent updating on prey spatial distribution, inadvertently communicated or not, should be particularly valuable for predators tracking ephemeral prey patches, providing an additional advantage to colonial living. Our results may have strong implications for cultural evolution in animal societies.

Fine-scale foraging behaviour of southern Buller’s albatross, the only Thalassarche that provisions chicks through winter

Predators generally time their reproductive events to match the peak in prey resource availability in order to sustain the elevated energy requirement of offspring provisioning. Consequently, most temperate/polar seabirds breed in spring/summer, including the majority of small albatross species that have short breeding cycles. In contrast, the southern Buller’s albatross Thalassarche bulleri bulleri has a delayed breeding schedule, with chick-rearing extending throughout the entire austral winter. In the present study, the fine-scale at-sea movements and trophic niche of chick-rearing southern Buller’s albatross were determined at Hautere/Solander Island (New Zealand, 46° 35’ S, 166° 54’ E) during the 2016 and 2017 chick-rearing periods to investigate the winter foraging strategy used during this nominally challenging period. The tracks recorded by 15 males (n = 43) and 11 females (n = 21) revealed that foraging behaviour accounted for only a small proportion of time at sea, primarily influenced by the time of day. Foraging occurred mainly in the neritic waters of New Zealand’s South Island shelf, with individuals undertaking consistent short trips (£ 230 km from the colony) or alternating short and long trips up to 1500 km from the colony. Fine-scale tracking data revealed that males spent more time foraging, during shorter trips than females. Their isotopic niches were small, with overlap between sexes, but with males having higher dN values than females. Time spent foraging was influenced by both static and dynamic oceanographic variables. These findings suggest that southern Buller’s albatross foraging behaviour, despite having to sustain chick provisioning in winter, is similar to that of summer-breeding congeners.

Divergent foraging strategies during incubation of an unusually wide-ranging seabird, the Murphy\u2019s petrel

Divergent foraging strategies may emerge within a population due to a combination of physiological and environmental factors; yet to persist, neither strategy should offer a consistent selective advantage over the alternative in the long term. Murphy’s petrels Pterodroma ultima from Henderson Island (24°20′S, 128°20′W) in the South Pacific Ocean are highly vagile, and exhibit two distinct foraging trip types during incubation; similar proportions of birds undertake either looping trips around the South Pacific Gyre to waters off Peru (hereafter “East”) or trips south-west of the colony towards the Subtropical Front (“South”) (mean maximum ranges of c. 3800 or 2000 km from the colony, respectively). However, the relative benefits of the distinct trip types remain unclear. Through tracking birds with GPS and salt-water immersion loggers in 2015, the fine-scale foraging behaviour was examined for East (trip durations: 14.1–19.8 days, maximum ranges 2387–4823 km) and South trips (12.9–25.8 days, 1565–1991 km). Data on behaviour classified from GPS tracks, the number of wet bouts per hour (a proxy for landing rates) and wind speeds, were used to distinguish two distinct foraging modes: birds on East trips spent more time in directed movement, whereas those on South trips spent a greater proportion of time in area-restricted search (ARS) behaviour. East trips were associated with higher overall mass gain, and wet bouts occurred in equal proportions during directed movement and ARS behaviour. This suggests that in unproductive marine environments, it may be more profitable to maximise area covered to increase the chances of encountering prey. Analysis of lower-resolution geolocator data (collected from 2011 to 2014) indicated that individuals were largely consistent in trip type between years. Since birds that conducted East trips were 19% lighter on departure from the colony and experienced more frequent tailwinds on foraging trips, we speculate that these birds may benefit from reduced movement costs, whilst also experiencing reduced competition for foraging opportunities.

Understanding the ontogeny of foraging behaviour: insights from combining marine predator bio-logging with satellite-derived oceanography in hidden Markov models.

The development of foraging strategies that enable juveniles to efficiently identify and exploit predictable habitat features is critical for survival and long-term fitness. In the marine environment, meso- and sub-mesoscale features such as oceanographic fronts offer a visible cue to enhanced foraging conditions, but how individuals learn to identify these features is a mystery. In this study, we investigate age-related differences in the fine-scale foraging behaviour of adult (aged ≥ 5 years) and immature (aged 2–4 years) northern gannets Morus bassanus. Using high-resolution GPS-loggers, we reveal that adults have a much narrower foraging distribution than immature birds and much higher individual foraging site fidelity. By conditioning the transition probabilities of a hidden Markov model on satellite-derived measures of frontal activity, we then demonstrate that adults show a stronger response to frontal activity than immature birds, and are more likely to commence foraging behaviour as frontal intensity increases. Together, these results indicate that adult gannets are more proficient foragers than immatures, supporting the hypothesis that foraging specializations are learned during individual exploratory behaviour in early life. Such memory-based individual foraging strategies may also explain the extended period of immaturity observed in gannets and many other long-lived species.

Reduced activity in middle-aged thick-billed murres: evidence for age related trends in fine-scale foraging behaviour

Several biological functions, such as reproductive success, peak during middle age in long-lived vertebrates. One possible mechanism for that peak is improved foraging performance during middle age, after a period of youthful inexperience and before senescence. Age may be particularly important in relating foraging behaviour to fitness for diving animals as altered skeletal muscle contraction efficiency or cardiovascular function could play a strong role at the scale of a single dive. Miniaturized accelerometers provide the opportunity to measure fine-scale foraging behaviour at the scale of a single wing beat. To examine the relationship between age and foraging behaviour in a diving seabird, whose reproductive success peaks during middle age, we equipped 115 thick-billed murres, Uria lomvia, with accelerometers and depth loggers. Murre activity (i.e. dynamic body acceleration) decreased with increasing dive depth during descent but increased with increasing maximum depth achieved. These patterns were inversed during ascent. After accounting for depth and maximum depth, middle-aged birds had low activity levels during the dive, compared with old and young birds, suggesting that old and young birds were less efficient at diving and foraging than middle-aged birds. Young individuals appeared to struggle at depths above 20 m during descent and throughout ascent when compared to middle-aged birds, while old individuals struggled at the end of deep dives during descent and during the initial parts of ascent when compared to the same middle-age class. We conclude that there is a link between foraging behaviour and age, contrary to previous findings. By examining foraging behaviour at a fine-scale, such as a dive, different energy expenditures across age groups were revealed, giving us insight on how seabirds are affected by senescence in the wild.

Intra-sexual variability in feeding behaviour of a mountain ungulate: size matters

Many studies comparing the behaviour of individuals of different genders or species showed that animal body mass and forage quality/quantity are key elements of the foraging ecology of herbivores. Since body mass could also influence the animal’s sensitivity to predation risk, its vigilance behaviour should consequently be affected. Alpine ibex (Capra ibex) is characterised by a strong dimorphism among males of different ages, thus representing an ideal case study for testing the Jarman-Bell principle, avoiding possibly misleading effects resulting from the comparison between different species or genders. We analysed the fine-scale foraging behaviour of male ibex in order to assess the effect of body mass and the effects of vegetation quality/quantity on both foraging and vigilance behaviour. Our results showed that smaller males were more selective than larger ones, on account of their lower capability of digesting plant. Smaller males scanned the environment more frequently than larger ones. Male ibex grazed more selectively in sites with high quality forage and their bite rate increased as forage biomass decreased. Vigilance frequency increased with increasing forage biomass as, under these circumstances, ibex are able to prolong anti-predator vigilance while chewing bites that have already been cropped. Our findings highlight the effects of body mass per se on both foraging and anti-predator behaviours in herbivores, thus supporting the Jarman-Bell principle. Foraging can arguably be considered a very flexible behaviour with high evolutionary relevance as it enables herbivores to optimally adjust their total energy intake under varying conditions of food resources.

Spatial scale and environmental determinants in minke whale habitat use and foraging

Because pelagic prey concentrations are patchy in both space and time, predators such as marine mammals require high degrees of flexibility in their habitat use. We tested the hypothesis that minke whales Balaenoptera acutorostrata adjust their habitat use during the feed- ing season at different spatial scales: their overall distribution should be determined by broad- scale oceanographic features, while foraging activity at finer scales should be dictated by short- term changes in habitat conditions. Results from generalized additive models indicate that minke whale distribution off the west coast of Scotland is dependent largely on temporally variable para- meters (sea surface temperature in spring, chlorophyll concentration in autumn), in addition to depth and topography. However, fine-scale foraging behaviour was dictated by the strength and direction of tidal currents. Seasonal distribution patterns according to environmental parameters were largely consistent between 2 different spatial scales, and over a time period of 15 yr. Signif- icantly higher sighting rates occurred in areas of predicted sandeel Ammodytes marinus presence in spring, but not during the rest of the summer, while in August and September, prey samples from the core study area consisted almost entirely of sprat Sprattus sprattus. The low energetic cost of swimming in minke whales and their ability to switch between different prey according to their seasonal availability thus appears to allow them to readily respond to temporal changes in pelagic prey concentrations at different scales. This occurs through a distribution influenced by temporally variable parameters (temperature and chlorophyll concentration), combined with adjustments in foraging activity dependent on variable conditions at fine spatial scales (tides).

Foraging ecology of black-backed woodpeckers (Picoides arcticus) in unburned eastern boreal forest stands

Managed coniferous forest dominates much of the black-backed woodpecker’s ( Picoides arcticus Swainson) breeding range. Despite this, little is known about the fine-scale foraging behaviour of this focal species in unburned managed forest stands in the absence of insect outbreaks. To investigate the foraging substrates used in such a habitat, we employed radio-telemetry to track a total of 27 black-backed woodpeckers. During two successive summers (2005–2006), 279 foraging observations were recorded, most of which were on dying trees, snags, and downed woody debris. Individuals frequently foraged by excavation, suggesting that in the absence of insect outbreaks the black-backed woodpecker forages mainly by drilling. The majority of foraging events occurred on recently dead snags with a mean dbh (±SE) of 18.3 ± 0.4 cm. Our results suggest that in unburned boreal forest stands, substrate diameter and decay class are important predictors of suitable foraging substrates for black-backed woodpeckers. We suggest that conservation efforts aimed at maintaining this dead-wood dependent cavity nesting species within the landscape, should endeavour to maintain 100 ha patches of old-growth coniferous forest. This would ensure the continuous production of a sufficient quantity of recently dead or dying trees to meet the foraging needs of this species.

Linear tracks and restricted temperature ranges characterise penguin foraging pathways

Marine predators are thought to follow sophisticated scale-dependent search strategies when seeking patchy and unpredictable prey. However, fine-scale information about these strategies has hitherto been difficult to obtain for diving predators that often remain at the sea surface for only limited periods of time. Using ARGOS telemetry and novel, low-powered, archival GPS, we followed the fine-scale at-sea behaviour of king penguins breeding on South Georgia. Results revealed that foraging pathways were generally linear, except at the finest scale, where movements probably reflected either fine-scale searching behaviour, or fine-scale random movements associated with having found prey. King penguins focused 45% of their foraging effort in waters with a specific surface temperature (5.0 to 5.5 degrees C) - an environmental cue potentially important in helping them locate prey, thereby reducing their need to expend energy in area-restricted search patterns. Within these waters, penguins slowed down and increased their dive effort and degree of meandering. First Passage Time analysis revealed that penguins focused much of their effort at local scales, generally in areas with a radius of 2 km. In these areas, penguins dived marginally deeper and targeted waters that, were significantly warmer at the bottom of their dives. Such information about fine-scale foraging behaviour will help increase our understanding of the environmental correlates that characterise areas where marine predators exploit their prey. The scale of these behavioural processes is better resolved using the fine-scale temporal and spatial resolution of GPS tracking data.

Pursuit plunging by northern gannets (Sula bassana) feeding on capelin (Mallotus villosus).

Northern gannets (Sula bassana) are considered to obtain prey usually by rapid, vertical, shallow plunge dives. In order to test this contention and investigate underwater foraging behaviour, we attached two types of data-logging systems to 11 parental northern gannets at Funk Island in the North-Wiest Atlantic. We documented, for the first time to the authors' knowledge, gannets performing long, flat-bottomed, U-shaped dives that involved underwater wing propulsion as well as rapid, shallow, V-shaped dives. The median and maximum dive depths and durations were 4.6 and 22.0 m and 8 and 38 s, respectively. Short, shallow dives were usually V-shaped and dives deeper than 8 m and longer than 10 s were usually U-shaped, including a period at constant depth (varying between 4 and 28s with median 8s). Diving occurred throughout the daylight period and deepest dives were performed during late morning. On the basis of motion sensors in the loggers and food collections from telemetered birds, we concluded that extended, deep dives were directed at deep schools of capelin, a small pelagic fish, and we hypothesized that V-shaped dives were aimed at larger, pelagic fishes and squids. Furthermore, these V-shaped dives allowed the birds to surprise their pelagic prey and this may be critical because the maximum swimming speeds of the prey species may exceed the maximum dive speeds of the birds.