Linking foraging behavior and diet in a diving seabird

Foraging behavior and diet of breeding seabirds may be analysed simultaneously with the combined use of remote sensing devices and stable isotope analysis. Imperial shag, Phalacrocorax atriceps, breeding at Punta León colony, Argentina, were equipped with global positioning system (GPS) loggers to record foraging trips and blood samples were taken after removal of the devices in order to analyse their nitrogen and carbon stable isotope composition in whole blood and plasma. Whole blood was correlated to plasma isotopic composition for each individual (n = 35), linking diet in the short and medium term. Sexes did not differ in isotopic signatures. The maximum distance reached and the total number of dives that individuals made on two consecutive foraging trips were correlated to their plasma nitrogen isotopic signature. Individuals that went further from the colony and dived fewer times presented more positive signatures, indicative of benthic prey consumption (e.g. Raneya brasiliensis). Diet was predominantly benthic with some individuals incorporating pelagic prey (Engraulis anchoita) and even cephalopods (Octopus tehuelchus). Within breeding pairs (n = 9), different combinations of foraging and prey preferences were observed. Estimated trophic levels of these individuals were similar to those of the same species in other colonies further south along the Patagonian coast.     

Habitat selection in birds feeding on ocean shores: landscape effects are important in the choice of foraging sites by oystercatchers

Food availability is a fundamental determinant of habitat selection in animals, including shorebirds foraging on benthic invertebrates. However, the combination of dynamic habitats, patchy distributions at multiple spatial scales, and highly variable densities over time can make prey less predictable on ocean‐exposed sandy shores. This can, hypothetically, cause a mismatch between prey and consumer distributions in these high‐energy environments. Here we test this prediction by examining the occurrence of actively foraging pied oystercatchers (Haematopus longirostris) in relation to physical habitat attributes and macrobenthic prey assemblages on a 34 km long, high‐energy beach in Eastern Australia. We incorporate two spatial dimensions: (i) adjacent feeding and non‐feeding patches separated by 200 m and (ii) landscape regions with and without foraging birds separated by 2–17 km. There was no support for prey‐based or habitat‐based habitat choice at the smaller dimension, with birds being essentially randomly distributed at the local scale. Conversely, at the broader landscape dimension, the distribution of oystercatchers was driven by the density of their prey, but not by attributes of the physical beach environment. This scale‐dependence suggests that, on open‐coast beaches, landscape effects modulate how mobile predators respond to variations in prey availability.     

Variability in the nutritional value of the major copepods in Cape Cod Bay (Massachusetts, USA) with implications for right whales

The North Atlantic right whale, a seriously endangered species, is found in Cape Cod Bay (Massachusetts, USA) during the winter and early spring. During their residency in these waters, these whales are frequently observed feeding. This study evaluated spatial and temporal changes in the chemical composition (carbon weight and C/N ratio) of the food resource targeted by the right whales in Cape Cod Bay. The three taxa measured (Centropages typicus, Pseudocalanus spp., and Calanus finmarchicus) had highly variable chemical compositions resulting from the different life strategies and from fluctuations in their surrounding environment. The impact of seasonal variability in the energy densities of the food resource of right whales was calculated and compared to the energetic requirements of these whales. Calculations indicated that differences in the nutritional content of the zooplankton prey in Cape Cod Bay could have a considerable effect on the nutrition available to the right whales. Therefore, it is likely that using more precise estimates of the energetic densities of the prey of right whales would lead to a re‐evaluation of the adequacy of the food resource available to these whales in the North Atlantic.     

Regular habitat switch as an important feeding strategy of an opportunistic seabird species at the interface between land and sea

During deteriorated prey availability, purely pelagic, specialised seabird species have to alter their feeding strategy by extending foraging radii and/or time spent at sea or reducing feeding intervals of chicks. In contrast, more generalised species such as the opportunistic black-headed gull (Larus ridibundus) breeding at the German North Sea coast, can be assumed to react on prey shortages by switching foraging habitats. The coastal zone of the German North Sea provides a rich habitat mosaic consisting of the offshore zone, tidal flats and terrestrial habitats. Thus, we expected distinct temporal and spatial patterns of habitat switch in accordance with prey availability and environmental constraints. We carried out ship-based and aerial surveys as well as dietary analyses and observations on flight activity. We found a significant switch from terrestrial to marine feeding sites both on a daily basis (related to tidal cycle) and over the whole breeding season. Most likely, the latter switch is the result of lower prey availability in the terrestrial habitats and an increasing quality (in terms of prey abundance and energy intake) of the marine area. While there was only moderate variability in habitat use among different years, we revealed significant differences in the diet of birds from different colonies. The high dietary plasticity and flexible feeding strategy, switching between terrestrial and marine prey is certainly of major importance for the success of an opportunistic avian top predator in a complex coastal zone. It is suggested that – compared to situations elsewhere – the number of breeding pairs of black-headed gulls in the German North Sea coast are still stable due to the switch of foraging habitats performed by individuals in this region.     

Small is profitable: No support for the optimal foraging theory in sea stars Asterias rubens foraging on the blue edible mussel Mytilus edulis

Doubt has been shed recently on the most popular optimal foraging theory stating that predators should maximize prey profitability, i.e., select that prey item that contains the highest energy content per handling time. We hypothesized that sea stars do not forage on blue mussels according to the classical optimal foraging theory but are actively avoiding damage that may be caused by e.g. capture of foraging on too-strong mussel shells, hence the sea stars will have a stronger preference for mussels that are smaller than the most profitable ones. Here we present experimental evidence of the sea star Asterias rubens as a predator that indeed chooses much smaller blue mussels Mytilus edulis to forage on than the most profitable ones. Hence this study does not support the optimal foraging theory. There may be other constraints involved in foraging than just optimizing energy intake, for example predators may also be concerned with preventing potential loss or damage of their foraging instruments.     

Vertical distribution and growth performance of Baltic cod larvae – Field evidence for starvation-induced recruitment regulation during the larval stage?

Besides variable egg survival, previous studies suggested that the larval stage may be the most critical phase in determining Baltic cod recruitment variability, and that larvae need to conduct an ontogenetic vertical migration from hatching depths (>50 m) to upper layers with increased food availability in order to initiate first feeding, improve their nutritional condition and growth, and avoid starvation. Recently, detailed information on the stage-resolved vertical distribution of main Baltic copepod species, including the preferred larval Baltic cod prey species Pseudocalanus acuspes, has become available. Therefore, the vertical distribution of Baltic cod larvae in August 2007 and their depth-dependent nutritional condition and growth were investigated. RNA–DNA based methods were used to estimate growth, including a novel approach to estimate growth performance by relating observed specific growth rates (SGR) of field caught larvae to temperature-dependent reference growth rates (G_ref) for fast-growing laboratory reared fish from the literature. This standardization to G_ref was found to have a great potential to improve investigations on the growth and ecology of larval fish. The need for early larvae to migrate to shallower layers was corroborated, while larger size classes were found at increasingly greater depths. This may reflect a continuation of the ontogenetic vertical migration in order to follow increasingly larger prey items at greater depths and to save energy in cooler waters below the thermocline. Larval growth generally declined with increasing depth, but the decline in growth became less pronounced in larger size classes. This indicates that larger larvae were better in coping with the ambient environment and the available prey field at greater depths. Generally, Baltic cod larvae grew poorly compared to larvae from other studies, which is discussed in relation to differences in predation and a possible food–temperature trade-off for larvae in the highly stratified Baltic Sea. Comparison with earlier results showed a higher frequency of starving larvae and lower frequencies of larger larvae after the first-feeding stage in 1994 and 1995. As this was a period of low Baltic cod recruitment despite favourable conditions for egg survival, it is concluded that larval starvation mortality has a high potential to contribute to recruitment variability in Baltic cod.     

Site-specific effects on productivity of an upper trophic-level marine predator: Bottom-up, top-down, and mismatch effects on reproduction in a colonial seabird

We investigated the relative roles of bottom-up and top-down factors in limiting productivity of an upper trophic level marine predator. Our primary working hypothesis was that the reproductive success of black-legged kittiwakes (Rissa tridactyla) a piscivorous, colonial-nesting seabird, was most limited by the abundance, distribution, and species composition of surface-schooling forage fishes. A secondary working hypothesis was that reproductive loss to kittiwake nest predators was greatest during years of reduced prey availability. We report on a broad-scale, integrated study of kittiwakes and their prey in Prince William Sound, Alaska. Our study spanned five breeding seasons (1995–1999) and focused on three colonies that differed in size (ranging from ca. 220 to ca. 7000 breeding pairs) and proximity to each other (50–135 km apart). Kittiwakes in PWS encountered a variety of aquatic habitats, creating a complex foraging environment for breeding birds. We measured kittiwake reproductive success and foraging activities, while simultaneously measuring the abundance of surface schooling forage fishes throughout the foraging range of breeding kittiwakes. The abundance of primary prey species for kittiwakes (Pacific herring Clupea pallasi, Pacific sand lance Ammodytes hexapterus, and capelin Mallotus villosus) varied both annually and regionally, with no one region consistently having the greatest abundance of prey. Likewise, kittiwake reproductive success varied considerably among colonies and years.We found that bottom-up, top-down, timing mismatch, and colony-specific effects were all important to kittiwake productivity. Although bottom-up effects appeared to be strongest, they were not evident in some cases until other effects, such as geographic location (proximity of colony to prey concentrations) and top-down predation, were considered. Important bottom-up effects on kittiwake reproductive success were not only total prey abundance and distribution, but also species, age composition, and chronology of prey occurrence (match/mismatch of timing with critical brood-rearing periods); these effects varied by colony.Top-down effects of predation on kittiwake nest contents (independent of prey abundance) confounded seabird-forage fish relationships. Ultimately, when confounding factors were minimized, non-linear asymptotic relationships were identified between kittiwakes and their prey, with an asymptotic threshold of fish school surface area density of ca. 5 m²/km², beyond which top-down, physiological, or phylogenetic constraints likely restrict further reproductive output. The integrated approach of our investigations provided a more thorough understanding of the mechanisms underlying predator–prey relationships in the complex marine environment. However, such mechanistic theories can only be tested and refined through long-term research and monitoring of much greater duration than the 5-year study reported herein.     

Foraging ecology of an endemic shorebird, the African Black Oystercatcher (Haematopus moquini) on the south–east coast of South Africa

We investigated small–medium (1–300 km) scale variation in the foraging ecology of the African Black Oystercatcher during its breeding season, using traditional diet analysis coupled with carbon and nitrogen stable isotope analysis. Fieldwork was conducted between January and March 2006 and 2007, on rocky shores on the south–east coast of South Africa at East London, Kenton and Port Elizabeth. Middens of shelled prey left by adults feeding their chicks were collected from five territories and the abundances of the collected prey on the foraging areas were estimated using quadrats. Blood samples from 45 birds (16 females, 10 males and 19 chicks) and tissues from the predominant prey species on the territory of each breeding pair were collected for isotope analysis. The Manly–Chesson selectivity index revealed that adults feed their chicks preferentially with the limpet Scutellastra cochlear and the Mediterranean mussel Mytilus galloprovincialis, if available. A slight enrichment in the ¹⁵N stable-carbon isotope signature was observed towards the west in both prey and oystercatchers. Differences in isotope signatures between males and females from the same breeding pair indicate sex-related differences in the diet. Both had signatures indicating a mixed diet, but with males exhibiting a signature closer to that of limpets and females closer to that of mussels. In the single case where mussels were rare on the feeding territory, the two members of a pair showed carbon signatures which were identical and very similar to that of limpets. These results indicate dietary partitioning between genders in breeding pairs.     

Predatory Promesostoma species (Plathelminthes, Rhabdocoela) in the Wadden Sea

Laboratory experiments were performed on the food ecology of four congeneric species of free-living plathelminths, Promesostoma caligulatum, P. marmoratum, P. rostratum, and P. meixneri, all inhabiting an intertidal sandflat near the island of Sylt (North Sea). Their prey spectrum is within the microcrustaceans: P. caligulatum preferred ostracods, while the other three species favoured copepods, with species-specific differences for copepod species and size classes. Daily consumption of prey species varied with the size of both the predator and the prey. On average, P. marmoratum consumed 0.76 Harpacticus flexus per day while this rate decreased to 0.06 in P. meixneri, the smallest predator. When these Promesostoma species were fed with Tachidius discipes, a smaller prey species, their predation rates were about 25% higher. While the larger predators preferred the larger harpacticoids as prey, the small P. meixneri preferred small cyclopoids over larger harpacticoids. In terms of biomass, P. marmoratum's mean consumption of T. discipes per day was about half the predator's own weight. This average varied with prey density and temperature. A comparison of these consumption rates with the field densities of the predators and their prey shows that the plathelminth predators may consume as much as 10% per day of their copepod prey populations, thus strongly influencing these prey populations on these sandflats. The predation pressure of P. caligulatum on ostracods was about 1% per day of the prey population. Since ostracods usually have fewer generations per year, the total effect on the population dynamics may be similar to that on copepods. Therefore, nocturnal swimming of copepods in the water column may be interpreted as an attempt to escape plathelminth predators.     

A hard-knock life: the foraging ecology of Cape cormorants amidst shifting prey resources and industrial fishing pressure

Once one of the most numerous seabirds of the Benguela upwelling system, the population of Cape cormorants Phalacrocorax capensis has decreased by 60% in the past three decades and the species is listed as Near Threatened. Declines in prey availability and/or abundance brought about by recent changes in the distribution of pelagic fish stocks and industrial purse-seine fishing are hypothesised to be a key driver of seabird population decreases in the southern Benguela. We investigated the foraging behaviour of breeding Cape cormorants by deploying GPS and temperature–depth recorders on 24 breeding adults from three islands off the coast of South Africa, two of them to the north of Cape Point and a third farther south on the western Agulhas Bank. This provided the first measures of foraging dispersal by a cormorant in the Benguela system, and enabled a comparison of foraging behaviour between birds from these islands. Foraging trips of Cape cormorants lasted between 17 min and >7 h, at a maximum distance of between 2 and 58 km away from their colony. Foraging effort was significantly greater for birds from farther north off the West Coast in terms of trip duration, distance travelled, number of dives and time spent flying compared to those from the southernmost island (Dyer), which is probably a response to low prey availability in the north. Coastal reserves that exclude pelagic fishing from inshore feeding grounds around Cape cormorant breeding colonies may result in increased local prey availability, which would benefit Cape cormorant populations.     

Diet of sardine Sardinops sagax in the southern Benguela upwelling ecosystem

The diet of sardine Sardinops sagax in the southern Benguela was investigated by microscopic examination of stomach contents. The relative dietary importance of prey size and prey type was assessed by calculating the carbon content of prey items. Sardine is an omnivorous clupeoid, ingesting both phytoplankton and zooplankton, with the relative importance of these two food types varying both spatially and temporally. Stomach contents were numerically dominated by small prey items, principally dinoflagellates, followed by crustacean eggs, cyclopoid copepods, calanoid copepods and diatoms. Virtually all prey items ingested by sardine were <1.2 mm maximum dimension, the particle size below which sardine only filter-feed. Despite the numerical dominance by phytoplankton, zooplankton contributed the major portion to sardine dietary carbon, small calanoid and cyclopoid copepods, anchovy eggs and crustacean eggs being the primary prey types. These results indicate that, like anchovy Engraulis capensis, sardine in the southern Benguela are primarily zoophagous, and contrast with earlier dietary studies on sardine in the region. However, the two species appear to partition their prey on the basis of size; sardine consume small zooplankton, whereas anchovy consume large zooplankton. This difference has been observed in other upwelling ecosystems where the two genera co-exist and is likely to contribute to the regime shifts observed between sardine and anchovy.     

Sex differences in body morphology and multitrophic interactions involving the foraging behaviour of the crab Carcinus maenas

Many animals are sexually dimorphic, but the underlying evolutionary causes and ecological consequences of sexual dimorphism are not fully understood. One predicted consequence for sexual dimorphism is that different sexes show niche differentiation. If sexual dimorphism is in feeding appendages, then differences may be manifested by different diets and thus contrasting behavioural responses to potential prey. Sexual dimorphisms in feeding appendages may also result in different handling times, which may then be correlated with differences in exposure, and, hence predation risk to the predator while feeding. In addition, the prey of the sexually dimorphic predator may respond differently to cues from each sex according to the predation risk each presents to the prey. We tested these predictions using a crab (Carcinus maenas) with sexual dimorphism in chelae dimensions, its predator the cuttlefish Sepia officinalis and prey with known differences in handling times; the gastropod molluscs Gibbula umbilicalis and Littorina littorea. We demonstrated that male C. maenas orientated more frequently to cues from L. littorea whereas females orientated more towards G. umbilicalis in contradiction of patterns predicted by handling times. Male crabs had a faster heart rate than females but this was not influenced by food‐based cues. We also showed no difference in foraging times with respect to changing levels of predator risk and also no differences in gastropod responses to odours from male or female crabs. Our results showed that predictions of handling time and sexual dimorphism are not associated. The experiments indicated the male and female crabs are probably ecological equivalents and thus niche differentiation is less likely.     

Seabird conservation and tidal stream and wave power generation: Information needs for predicting and managing potential impacts

Current development plans indicate that during the next decade there will be an increase in tidal stream and wave (TSW) power generation activity in Scottish Waters, together with the designation of additional offshore areas for seabird conservation. This paper summarises how TSW developments could affect seabirds, based on experience from other forms of disturbance, and explores the possible changes in behaviour and habitat that have the potential to increase a seabird's rate of energy acquisition (e.g. through enhancing prey abundance), or energy expenditure (e.g. through causing birds to commute further to find food, if they avoid foraging around developments placed in regular feeding areas). Changes to energy budgets could impact rates of reproduction and survival. Simulation modelling of seabird energetics and behaviour is one possible tool for predicting the direction and magnitude of population impacts caused by alterations to energy budgets, but is dependant on the availability and accuracy of necessary parameters. The later sections of the paper review the information needed for such models and shows that although some data are available regarding rates of energy expenditure during specific activities, more information is needed on seabird foraging rates. The paper also highlights how the susceptibility of a species to be impacted by future TSW development is likely to be related to their method of foraging, flight behaviour and ability to buffer against environmental fluctuations.     

Energy profiling of demersal fish: A case-study in wind farm artificial reefs

The construction of wind farms introduces artificial hard substrates in sandy sediments. As Atlantic cod (Gadus morhua) and pouting (Trisopterus luscus) tend to aggregate in order to feed around these reefs, energy profiling and trophic markers were applied to study their feeding ecology in a wind farm in the Belgian part of the North Sea. The proximate composition (carbohydrates, proteins and lipids) differed significantly between liver and muscle tissue but not between fish species or between their potential prey species. Atlantic cod showed to consume more energy than pouting. The latter had a higher overall energy reserve and can theoretically survive twice as long on the available energy than cod. In autumn, both fish species could survive longer on their energy than in spring. Polyunsaturated fatty acids were found in high concentrations in fish liver. The prey species Jassa and Pisidia were both rich in EPA while Jassa had a higher DHA content than Pisidia.Energy profiling supported the statement that wind farm artificial reefs are suitable feeding ground for both fish species. Sufficient energy levels were recorded and there is no indication of competition.     

Observations on the predatory behaviour of the sevengill shark Notorynchus cepedianus

Studies on the feeding behaviour of large predatory sharks are inherently problematic because of the size of the animals, the difficulty in observing and handling them and the risks to the investigator. Observations on the feeding behaviour of the sevengill shark Notorynchus cepedianus over a seven-year period revealed this species to display at least four distinct foraging strategies. A particular strategy, or a combination of two or more, was employed depending on the size and type of prey being subdued. The four primary factors that appear to influence prey selection were prey size, availability and density, and scavenging. The behaviour of a prey species influences the predator's foraging and hunting behaviour. The success of the sevengill shark as an apical predator can be attributed, in part, to the feeding strategies it employs to subdue prey.     

Feeding ecology of the mud shrimp Solenocera melantho in the East China Sea

The feeding habits of the mud shrimp Solenocera melantho were studied in the East China Sea by analysing 720 stomach contents and comparing diet composition and prey diversity among seasons, sexes and size classes. Feeding activity was linked to season and ovarian condition. The stomach fullness was high during spring and summer and low in fall. Females with advanced ovaries also displayed low stomach fullness, which suggests that feeding activity is affected by the reproductive cycle. The diet of S. melantho consisted of 42 different prey categories, primarily smaller crustaceans, Foraminifera, polychaetes, mollusks and fishes (larvae and eggs). Crustacea,Foraminifera and polychaetes together constituted the dominant prey groups, accounting for 75% of total prey abundance and >50% of total prey occurrence. Diet composition differed among seasons between sexes and size classes. Females and males consumed the same prey items but with different orders of importance. In terms of body size, the small shrimps preferred relatively small food items, such as Foraminifera and algae, whereas larger shrimps preferred polychaetes and crustaceans. Trophic diversity varied among the seasons within both sexes and size classes, with the highest values being observed in fall. Niche overlap was high within both sexes and size classes among seasons (0.6051–0.8740).     

Dusky dolphins Lagenorhynchus obscurus and Cape fur seals Arctocephalus pusillus pusillus: fatty acid composition of their blubber and prey species

The fatty acid composition of the blubber of five dusky dolphins Lagenorhynchus obscurus and five Cape fur seals Arctocephalus pusillus pusillus from the northern Benguela ecosystem (South-East Atlantic) and their main prey was determined. Differences in fatty acid composition of the inner and outer blubber layer of the dolphins were substantial, with higher relative amounts of monoenic fatty acids with 14, 16 and 18 carbons in the outer layer and higher relative amounts of saturated, long-chain monounsaturated and polyunsaturated fatty acids in the inner layer. This stratification is similar to the general pattern that has been observed in a variety of marine mammals, but the degree of stratification is the highest yet observed, with the long-chained (n3) fatty acids being more than 20 times more abundant in the inner than in the outer layer. On the other hand, the seals’ blubber consisted of only one uniform layer, densely supported by connective tissue. The whole-body fatty acid composition of the prey was species specific. The dolphins and seals had significantly different fatty acid composition of their blubber. In both species, the blubber fatty acid composition was different from the composition of the prey, indicating that a phylogenetic component is involved in the determination of the fatty acid composition of the blubber.     

Scales of predator detection behavior and escape in Fissurella limbata: A field and laboratory assessment

The consumptive effects of predators are widely acknowledged, but predation can also impact prey populations through non‐consumptive effects (NCEs) such as costly antipredator behavioral responses. The magnitude of antipredator behavioral responses by prey is determined by an assessment of risk using sensory cues, which in turn is modulated by the environmental context. We studied the detection behavior and escape response of the keyhole limpet Fissurella limbata from the predatory sea star Heliaster helianthus. Through laboratory and field experimental trials, we quantified the distance and time of predator detection behavior by the prey, and measured their active escape responses when elicited. We found that predator detection by the limpet was chiefly mediated by distance, with experimental individuals capable of detecting predator presence effectively up to distances of at least 50 cm in the field and 70 cm under laboratory conditions. Our results indicate that this prey species is able to evaluate the proximity of its predator and use it as an indication of predation risk; therefore, predator–prey distance appears to be a primary predictor of the magnitude of the antipredator response. Given the tight relationship between predator distance and prey movement and the important role herbivores can play, particularly in this ecosystem, we expect that NCEs will cascade to the patterns of abundance and composition of rocky shore communities through changes in prey foraging behavior under risk.     

Two new species of the marine genus Limnodriloides and a record of Tubificoides fraseri Brinkhurst (Oligochaeta: Tubificidae) from New Zealand

We characterised seasonal and ontogenetic changes in diet and prey energy density of rainbow trout (Oncorhynchus mykiss) in Lake Rotoiti, New Zealand, to better understand the prey requirements of trout in central North Island lakes. Common smelt (Retropinna retropinna) was the dominant prey item of rainbow trout larger than 200 mm (77.8% of diet by weight), followed by kōura (freshwater crayfish Paranephrops planifrons; 6.3%), common bully (Gobiomorphus cotidianus; 5.5%), and kōaro (Galaxias brevipinnis; 3.4%). Juvenile rainbow trout (<200 mm) consumed amphipods, aquatic and terrestrial insects, oligochaetes, tanaid shrimps, and smelt. Trout consumed kōaro only in autumn and winter; consumption of other species did not vary seasonally. The maximum size of smelt consumed increased with increasing trout size, but trout continued to consume small smelt even as large adults. Consumption of larger prey items (kōaro and kōura) also increased with increasing trout size. This study indicates the importance of smelt for sustaining rainbow trout populations, as predation on other species was relatively low. These findings provide a basis for bioenergetic modelling of rainbow trout populations in lakes of the central North Island of New Zealand.