EFFECTS OF MEAL SIZE ON OTOLITH RECOVERY FROM FECAL SAMPLES OF GRAY AND HARBOR SEAL PUPS

Recovered otoliths from pinniped feces provide valuable information on diet composition and prey size. We studied the effect of meal size on otolith recovery from the feces of one harbor and eight gray seal pups. Each of 11 experiments comprised a half-ration meal, a period of fecal collection, a 1.5-or double-ration meal again followed by a period of fecal collection. A significantly lower percentage of Atlantic herring otoliths were recovered from half-ration meals (25%± 12.5% in the harbor seal, 8.6%± 6.9% in eight gray seals) than from 1.5- or double-ration meals (62.5%± 3.1 % in the harbor seal, 32.8%± 23.5% in gray seals). Meal size also significantly affected the percentage of Atlantic cod otoliths recovered from gray seal feces (65.0%± 26.3% from half ration, 98.3%± 2.9% from 1.5 ration). For both size meals, recovered cod otoliths were more significantly eroded than herring otoliths. The development of correction factors to account for the effects of digestion will need to consider the distribution of meal sizes of free-ranging pinnipeds.     

Ecological costs of climate change on marine predator–prey population distributions by 2050

Identifying and quantifying the effects of climate change that alter the habitat overlap of marine predators and their prey population distributions is of great importance for the sustainable management of populations. This study uses Bayesian joint models with integrated nested Laplace approximation (INLA) to predict future spatial density distributions in the form of common spatial trends of predator–prey overlap in 2050 under the “business‐as‐usual, worst‐case” climate change scenario. This was done for combinations of six mobile marine predator species (gray seal, harbor seal, harbor porpoise, common guillemot, black‐legged kittiwake, and northern gannet) and two of their common prey species (herring and sandeels). A range of five explanatory variables that cover both physical and biological aspects of critical marine habitat were used as follows: bottom temperature, stratification, depth‐averaged speed, net primary production, and maximum subsurface chlorophyll. Four different methods were explored to quantify relative ecological cost/benefits of climate change to the common spatial trends of predator–prey density distributions. All but one future joint model showed significant decreases in overall spatial percentage change. The most dramatic loss in predator–prey population overlap was shown by harbor seals with large declines in the common spatial trend for both prey species. On the positive side, both gannets and guillemots are projected to have localized regions with increased overlap with sandeels. Most joint predator–prey models showed large changes in centroid location, however the direction of change in centroids was not simply northwards, but mostly ranged from northwest to northeast. This approach can be very useful in informing the design of spatial management policies under climate change by using the potential differences in ecological costs to weigh up the trade‐offs in decisions involving issues of large‐scale spatial use of our oceans, such as marine protected areas, commercial fishing, and large‐scale marine renewable developments.     

Seasonal and regional variations in the feeding habits of the harbour seal, Phoca vitulina, in the Skagerrak and the Kattegat

Studies of the feeding of harbour seals have been carried out at the Tjärnö Marine Biological Laboratory since 1977. The studies are based on fish otoliths found in faeces at seal haulouts. The present paper compares feeding habitats at two different localities. Three families of fish, gadoids, pleuronectids and clupeoids were predominant in the seals' diet at a rocky shore habitat. Pleuronectids made up 75% of the diet at a sandy shore habitat. Temporal variations in feeding habits are also examined. The results indicate that harbour seals are opportunists in their choice of prey species, but some locally abundant species do not appear in their diet.     

Harp seal foraging behaviour during summer around Svalbard in the northern Barents Sea: diet composition and the selection of prey

The harp seal Pagophilus groenlandicus is a major high trophic level predator in the Barents Sea, and to better understand their function in the Barents Sea ecosystem, we need to understand their foraging behaviour during their most intensive feeding period. We analysed the diet composition and prey preference of 184 harp seals and 94 faeces samples, sampled in the northern Barents Sea (around Svalbard) during the period May–August in 1996, 1997, and 2004–2006. Concurrent with the sampling of seals, prey availability was assessed in one area in 1996 and 1997 and in two areas in 2006 using standard acoustic methods. Our study showed that harp seal diet composition varied significantly both in time (year) and space, and that their diets appeared to be size dependent. Both subadult (<150 cm) and adult seals were associated with pelagic crustaceans (particularly krill), whereas primarily adult seals were associated with fish (capelin, gadoids and flatfish). Krill was the most important prey group (63 %) followed by polar cod (16 %) and other fish species (10 %). The prey preference of harp seals varied in time and space; polar cod was often preferred by the seals whereas krill was commonly consumed in lower proportion than observed in the survey area. Gadoids and capelin had either been exploited in the same or less proportion as observed in the survey sea. This study emphasises the ecological significance of krill as prime food for harp seals during their intensive feeding period in summer.     

FEEDING METHOD AFFECTS OTOLITH DIGESTION IN CAPTIVE GRAY SEALS: IMPLICATIONS FOR DIET COMPOSITION ESTIMATION

Analysis of prey structures from scats has become widely used for assessing the diet of free-ranging seals. Captive feeding experiments have played an important role in the development of scat analysis but methodology has varied. We investigated whether using an experimental otolith-carrier species or in situ otolith experimental prey to feed haddock, plaice, and sand eel otoliths to two captive gray seals affected the amount of otolith digestion, and therefore our ability to estimate fish size and diet composition. Otolith recovery rates varied among the three prey species, but were not affected by feeding method. Otoliths were more digested in carrier experiments; resulting digestion coefficients were greater than those from in situ experiments. As a result, while the lengths of whole fish fed experimentally could be accurately predicted by applying in situ digestion coefficients, the lengths of these fish could not be accurately predicted using carrier digestion coefficients. Consequently, the estimated proportion by weight of each species in the diet can change markedly when carrier, as opposed to in situ , digestion coefficients are used. The implications for diet composition estimation are significant.     

Diet composition and food consumption rate of harbor porpoises (Phocoena phocoena) in the western Baltic Sea

Stomach content composition and prey‐specific consumption rates of juvenile and adult harbor porpoises (Phocoena phocoena) were estimated from a data set including 339 stomachs collected over a 32 yr period (1980–2011) in the western Baltic Sea. The stomach contents were mainly hard parts of fish prey and in particular otoliths. The bias originating from differential residence time of otoliths in the stomachs was addressed by use of a recently developed approach. Atlantic cod and herring were the main prey of adults, constituting on average 70% of the diet mass. Juvenile porpoises also frequently consumed gobies. Here, the mass contribution by gobies was on average 25%, which was as much as cod. Other species such as whiting, sprat, eelpout, and sandeels were of minor importance for both juveniles and adults. The diet composition differed between years, quarters, and porpoise acquisition method. Yearly consumption rates for porpoises in the western Baltic Sea were obtained in three scenarios on the daily energy requirements of a porpoise in combination with an estimate including the 95% CLs of the porpoise population size. Cod of age groups 1 and 2 and intermediate‐sized herring suffered the highest predation from porpoises.     

Assessment of errors associated with harbour seal (Phoca vitulina) faecal sampling

Six harbour seals, ages 4–8 years, were held as pairs in a 10 times 20 times 2 m tank filled with sea water, and on 60 occasions were fed a meal of a specific species of fish or cephalopod of known size. The tank was drained periodically, and harbour seal faeces were collected on a 0.5 mm sieve. Number and size of otoliths and beaks found in faeces were determined. Fifty-eight percent of 670 fish and 37% of 36 cephalopods fed to harbour seals were represented by their otoliths or beaks in faeces. Estimated number of prey consumed was determined from the greatest number of left or right otoliths or upper or lower beaks collected in faeces. Estimated length ofprey was determined from measurements of otoliths and beaks recovered in the tank and relationships of otolith and beak measurements to prey length. Estimated number of fish eaten was not significantly different among pairs of harbour seals, but was different among species of fishes. Only 24–35% of fish species with small otoliths were represented in faeces, whereas more robust otoliths from other species were less apt to be completely dissolved. Estimated length of fishes was significantly less than lengths of fishes fed to harbour seals in 39 (76.5%) of 51 trials. Cephalopod beaks were not affected by passage through the harbour seal digestive tract. Amount of otolith dissolution was not related to species of fish; estimated fish length was underestimated by an average 27.5%. Although some (7.4%) of the otoliths were collected within 100 h after the fish were ingested, more than 90% were recovered within 24 h after the fish was eaten. Correction factors were developed which will allow researchers to estimate more reliably number and size of fish and cephalopod prey eaten by harbour seals.     

Food habits of harbor seals (Phoca vitulina richardii) as an indicator of invasive species in San Francisco Bay,California

The diet of harbor seals (Phoca vitulina richardii) in San Francisco Bay (SFB), California, was determined from July 2007 to July 2008 using prey hard parts recovered from 442 scats collected at five haul‐out sites. Twenty‐two species of fish and one species of crustacean were identified, but harbor seals primarily ate a nonnative invasive species, yellowfin goby (Acanthogobius flavimanus), which increased in dietary importance since the diet was last studied in 1991/1992. Additionally, another nonnative invasive fish species, chameleon goby (Tridentiger trigonocephalus), was found for the first time in the diet of harbor seals in SFB. Harbor seal diet was statistically different between years (1991/1992 and 2007/2008), between the pupping and nonpupping seasons, and between North SFB and South SFB haul‐out locations. The diet of harbor seals was significantly correlated with fish species caught in trawl surveys conducted by the California Department of Fish and Wildlife (CDFW) during the same time periods as this study (2007/2008). Harbor seals currently are influencing the health of the SFB ecosystem in a positive manner by consuming large quantities of nonnative invasive fish species.     

Otolith size and location in digestive tracts of northern fur seals (Callorhinus ursinus): Implications for dietary interpretations

Walleye pollock (Theragra chalcogramma) otoliths (n= 2,706) recovered from stomachs, small intestines, and colons of 43 northern fur seals (Callorhinus ursinus) were evaluated for size and wear by location in the digestive tract. Pollock fork length was regressed on otolith length after correction for erosion, and age was estimated from the calculated body size. Age‐1+ pollock otoliths (≥6.3‐mm length) were concentrated in stomachs while age‐0 otoliths (≤6.2‐mm length) were concentrated in colons. Less than 10% of otoliths were found in the small intestines. Pollock age decreased with progression along seal gastrointestinal tracts. Otolith quality increased along gastrointestinal tracts in numbers ≥20, which was typical of age‐0 otoliths recovered from colons. Otolith distribution by age and quality along gastrointestinal tracts suggests that small (≤12 cm) schooling prey are consumed in large volume and passed as a bolus rapidly through the digestive tract before significant erosion of bony remains occurs; while larger prey are eaten in smaller volume and subjected to otolith erosion due to longer retention in the stomach. Our results illustrate the importance of multiple sampling strategies to comprehensively represent prey size in pinniped diet.     

Large‐scale molecular barcoding of prey DNA reveals predictors of intrapopulation feeding diversity in a marine predator

Predator–prey interactions are critical in understanding how communities function. However, we need to describe intraspecific variation in diet to accurately depict those interactions. Harbor seals (Phoca vitulina) are an abundant marine predator that prey on species of conservation concern. We estimated intrapopulation feeding diversity (variation in feeding habits between individuals of the same species) of harbor seals in the Salish Sea. Estimates of feeding diversity were examined relative to sex, month, and location using a novel approach that combined molecular techniques, repeated cross‐sectional sampling of scat, and a specialization metric (within‐individual consistency in diet measured by the Proportional Similarity Index ()). Based on 1,083 scat samples collected from five haul‐out sites during four nonsequential years, we quantified diet using metabarcoding techniques and determined the sex of the scat depositor using a molecular assay. Results suggest that intrapopulation feeding diversity was present. Specialization was high over short periods (24–48 hr,  = 0.392, 95% CI = 0.013, R = 100,000) and variable in time and space. Females showed more specialization than males, particularly during summer and fall. Additionally, demersal and benthic prey species were correlated with more specialized diets. The latter finding suggests that this type of prey likely requires specific foraging strategies and that there are trade‐offs between pelagic and benthic foraging styles for harbor seals. This differential feeding on prey species, as well as between sexes of harbor seals, indicates that predator–prey interactions in harbor seals are complex and that each sex may have a different impact on species of conservation concern. As such, describing intrapopulation feeding diversity may unravel hitherto unknown complex predator–prey interactions in the community.     

A captive feeding study with the Pacific harbor seal (Phoca vitulina richardii): Implications for scat analysis

Seven prey species ( n _total > 2,700) were fed to seven captive male Pacific harbor seals ( Phoca vitulina richardii ) in 177 experimental meals to quantify biases associated with scat analysis and current consumption models. Hard parts from an individual meal were recovered in an average of 3.8 ± 1.8 scats (range 1–10; mean ± SD). Overall, 57.7 ± 33.2% of otoliths and 89.5 ± 15.5% of squid beaks were recovered. Recovery rates varied, and prey with smaller, fragile otoliths were recovered in lesser quantities than prey with larger, robust otoliths. Recovery rates of all prey except pink salmon were improved by a mean of 31.7% when all diagnostic structures were included in estimates. Estimated recovery of pink salmon was 9.5 times that fed seals based on the all-structure technique. Mean length reduction of recovered otoliths was 20.4 ± 10.1%. Correction factors calculated from average length reduction improved length estimates for all fish species. Grade-specific length correction factors (gLCFs) reduced variability in all of the estimates and significantly improved estimates of prey with highly eroded otoliths including Pacific hake and shortbelly rockfish. The Biomass Reconstruction (BR) model accurately predicted biomass consumption within 4% of known consumption, whereas estimates based on frequency of occurrence were inaccurate.     

Fish diet of the Antarctic fur seal,Arctocephalus gazella,in summer,at Stranger Point,King George Island,South Shetland Islands

 In February 1992, 34 faecal samples from non-breeding male Antarctic fur seals, Arctocephalus gazella, were collected at Stranger Point, King George Island, South Shetlands. Fish constituted an important part of the diet, occurring in 90% of those scats containing prey remains. From 1162 otoliths found in the faeces, 1086 were identified to at least family level. Myctophids and nototheniids represented together almost 90% of the fish eaten. The dominant species were Gymnoscopelus nicholsi, Pleuragramma antarcticum and Electrona antarctica, contributing 33.3%, 30.8% and 12.0% of the otoliths respectively. The standard length of these three species was estimated from otoliths with little or no signs of erosion. This study showed that fur seals fed mainly on pelagic fish species that are often associated with krill. These findings are corroborated by fur seal diving patterns. Received: 7 October 1994/Accepted: 5 October 1995     

Using the otolith sulcus to aid in prey identification and improve estimates of prey size in diet studies of a piscivorous predator

Diet studies are fundamental for understanding trophic connections in marine ecosystems. In the southeastern US, the common bottlenose dolphin Tursiops truncatus is the predominant marine mammal in coastal waters, but its role as a top predator has received little attention. Diet studies of piscivorous predators, like bottlenose dolphins, start with assessing prey otoliths recovered from stomachs or feces, but digestive erosion hampers species identification and underestimates fish weight (FW). To compensate, FW is often estimated from the least affected otoliths and scaled to other otoliths, which also introduces bias. The sulcus, an otolith surface feature, has a species‐specific shape of its ostium and caudal extents, which is within the otolith edge for some species. We explored whether the sulcus could improve species identification and estimation of prey size using a case study of four sciaenid species targeted by fisheries and bottlenose dolphins in North Carolina. Methods were assessed first on otoliths from a reference collection (n = 421) and applied to prey otoliths (n = 5,308) recovered from 120 stomachs of dead stranded dolphins. We demonstrated in reference‐collection otoliths that cauda to sulcus length (CL:SL) could discriminate between spotted seatrout (Cynoscion nebulosus) and weakfish (Cynoscion regalis) (classification accuracy = 0.98). This method confirmed for the first time predation of spotted seatrout by bottlenose dolphins in North Carolina. Using predictive models developed from reference‐collection otoliths, we provided evidence that digestion affects otolith length more than sulcus or cauda length, making the latter better predictors. Lastly, we explored scenarios of calculating total consumed biomass across degrees of digestion. A suggested approach was for the least digested otoliths to be scaled to other otoliths iteratively from within the same stomach, month, or season as samples allow. Using the otolith sulcus helped overcome challenges of species identification and fish size estimation, indicating their potential use in other diet studies.     

Fish prey of Antarctic fur seals Arctocephalus gazella at Ile de Croy,Kerguelen

 The composition of Antarctic fur seal prey was assessed through analysis of scats collected in March 1994 on Ile de Croy, Iles Nuageuses. Fish remains predominated in samples, occurring in 95% of droppings. A total of 968 otoliths allowed the identification of 16 fish species. Myctophid fish (12 species) dominated the diet both by number (94% of the otoliths) and by fish reconstituted mass (76%). Three fish species constituted together 87% of the reconstituted mass: the myctophids Gymnoscopelus nicholsi (52%) and G. piabilis (12%), and the channichthyid Champsocephalus gunnari (23%). Prey distribution suggests that during late summer seals forage in upper slope waters in the northeast of the Kerguelen Archipelago. Received:1 March 1996/Accepted: 20 May 1996     

Identification of hairs found in leopard seal (<Emphasis Type="Italic">Hydrurga leptonyx</Emphasis>) scats

The leopard seal is a top-order predator in the Southern Ocean ecosystem and preys on a wide variety of vertebrate species including seals and penguins. We assessed the use of hairs found in leopard seal scats to identify the species of pinniped consumed. A reference collection of hairs was obtained from four potential leopard seal prey species including crabeater, Weddell, Ross, and Southern elephant seals. Discrimination techniques applied to terrestrial mammals did not allow for identification of the seal hairs. Instead, a 2-dimensional (2-D) and 6-dimensional (6-D) analysis technique utilising Mahalanobis distances (D ²) was used. The smallest Mahalanobis distance together with the largest value of p(F) positively identified hairs from each species. The 6-D analysis was more accurate and applied to hairs found in the leopard seal scats. The majority of prey species were identified as crabeater seals, which are a known prey item of the leopard seal.     

Bayesian joint models with INLA exploring marine mobile predator–prey and competitor species habitat overlap

Understanding spatial physical habitat selection driven by competition and/or predator–prey interactions of mobile marine species is a fundamental goal of spatial ecology. However, spatial counts or density data for highly mobile animals often (1) include excess zeros, (2) have spatial correlation, and (3) have highly nonlinear relationships with physical habitat variables, which results in the need for complex joint spatial models. In this paper, we test the use of Bayesian hierarchical hurdle and zero‐inflated joint models with integrated nested Laplace approximation (INLA), to fit complex joint models to spatial patterns of eight mobile marine species (grey seal, harbor seal, harbor porpoise, common guillemot, black‐legged kittiwake, northern gannet, herring, and sandeels). For each joint model, we specified nonlinear smoothed effect of physical habitat covariates and selected either competing species or predator–prey interactions. Out of a range of six ecologically important physical and biologic variables that are predicted to change with climate change and large‐scale energy extraction, we identified the most important habitat variables for each species and present the relationships between these bio/physical variables and species distributions. In particular, we found that net primary production played a significant role in determining habitat preferences of all the selected mobile marine species. We have shown that the INLA method is well‐suited for modeling spatially correlated data with excessive zeros and is an efficient approach to fit complex joint spatial models with nonlinear effects of covariates. Our approach has demonstrated its ability to define joint habitat selection for both competing and prey–predator species that can be relevant to numerous issues in the management and conservation of mobile marine species.     

Feeding habits of three seal species at the Danco Coast, Antarctica: a re-assessment

The analysis of prey overlap among Weddell, Antarctic fur and leopard seals was conducted using fecal samples collected at the Danco Coast, Antarctic Peninsula, in 1998 and 2000. The re-occurrence of prey species was moderate in samples collected in 1998, and low in 2000, and reflects resource partitioning among seal species. Prey species that mostly co-occurred in seals’ diet were the Antarctic krill Euphausia superba, bivalves, and the myctophids Gymnoscopelus nicholsi and Electrona antarctica. A dietary similarity index of prey overlap has been calculated and demonstrates evident fluctuations in pairwise comparisons between the seal species. The highest and lowest values of prey overlap were observed between Antarctic fur seals and leopard seals, and between Weddell seals and leopard seals, respectively. Prey overlap between Antarctic fur seals and Weddell seals was moderate in both seasons.     

THE TROPHIC ROLE OF MARINE MAMMALS IN THE NORTHERN GULF OF ST. LAWRENCE

The trophic role of apex predators was evaluated in the northern Gulf of St. Lawrence ecosystem. An Ecopath model was developed for the period 1985–1987 prior to the collapse of commercially exploited demersal fish stocks in this area. Marine mammal trophic levels were estimated by the model at 4.1 for cetaceans, 4.4 for harp seals (Pagophilus groenlandicus), 4.7 for hooded seals (Cystophora cristata), 4.5 for gray seals (Halichoerus grypus), and 4.3 for harbor seals (Phoca vitulina). Harp seals were the third most important predator on vertebrate prey following large Atlantic cod (Gadus morhua) and redfish (Sebastes spp.). Different seal species preyed on different levels of the food chain. Harp seals preyed on most trophic groups, whereas larger seals, such as gray seals and hooded seals, mainly consumed higher trophic levels. The model suggested that apex predators had a negative effect on their dominant prey, the higher trophic level fish, but an indirect positive feedback on the prey of their preferred prey, mainly American plaice (Hippoglossoides platessoides), flounders, skates, and benthic invertebrates. Our results suggest that both marine mammals and fisheries had an impact on the trophic structure.     

Latitudinal variation in ecological opportunity and intraspecific competition indicates differences in niche variability and diet specialization of Arctic marine predators

Individual specialization (IS), where individuals within populations irrespective of age, sex, and body size are either specialized or generalized in terms of resource use, has implications on ecological niches and food web structure. Niche size and degree of IS of near‐top trophic‐level marine predators have been little studied in polar regions or with latitude. We quantified the large‐scale latitudinal variation of population‐ and individual‐level niche size and IS in ringed seals (Pusa hispida) and beluga whales (Delphinapterus leucas) using stable carbon and nitrogen isotope analysis on 379 paired ringed seal liver and muscle samples and 124 paired beluga skin and muscle samples from eight locations ranging from the low to high Arctic. We characterized both within‐ and between‐individual variation in predator niche size at each location as well as accounting for spatial differences in the isotopic ranges of potential prey. Total isotopic niche width (TINW) for populations of ringed seals and beluga decreased with increasing latitude. Higher TINW values were associated with greater ecological opportunity (i.e., prey diversity) in the prey fish community which mainly consists of Capelin (Mallotus villosus) and Sand lance (Ammodytes sp.) at lower latitudes and Arctic cod (Boreogadus saida) at high latitudes. In beluga, their dietary consistency between tissues also known as the within‐individual component (WIC) increased in a near 1:1 ratio with TINW (slope = 0.84), suggesting dietary generalization, whereas the slope (0.18) of WIC relative to TINW in ringed seals indicated a high degree of individual specialization in ringed seal populations with higher TINWs. Our findings highlight the differences in TINW and level of IS for ringed seals and beluga relative to latitude as a likely response to large‐scale spatial variation in ecological opportunity, suggesting species‐specific variation in dietary plasticity to spatial differences in prey resources and environmental conditions in a rapidly changing ecosystem.     

Harbor seal population decline in the Aleutian Archipelago

Populations of Steller sea lions, northern fur seals, and northern sea otters declined substantially during recent decades in the Bering Sea and Aleutian Islands region, yet the population status of harbor seals has not been assessed adequately. We determined that counts obtained during skiff‐based surveys conducted in 1977–1982 represent the earliest estimate of harbor seal abundance throughout the Aleutian Islands. By comparing counts from 106 islands surveyed in 1977–1982 (8,601 seals) with counts from the same islands during a 1999 aerial survey (2,859 seals), we observed a 67% decline over the ～20‐yr period. Regionally, the largest decline of 86% was in the western Aleutians (n= 7 islands), followed by 66% in the central Aleutians (n= 64 islands), and 45% in the eastern Aleutians (n= 35 islands). Harbor seal counts decreased at the majority of islands in each region, the number of islands with >100 seals decreased ～70%, and the number of islands with no seals counted increased ～80%, indicating that harbor seal abundance throughout the Aleutian Islands was substantially lower in the late 1990s than in the 1970s and 1980s.