Behavioral effects of environmental enrichment on harbor seals (Phoca vitulina concolor) and gray seals (Halichoerus grypus)

Zoos and aquariums have been incorporating environmental enrichment into their animal care programs for the past 30 years to increase mental stimulation and promote natural behaviors. However, most attempts to document the effects of enrichment on animal behavior have focused on terrestrial mammals. Staff at the National Aquarium in Baltimore conducted an investigation of the behavioral effects of enrichment on the seven harbor seals and two gray seals housed in the aquarium's outdoor seal exhibit. We expected that enrichment would change the amount of time the animals spent engaged in specific behaviors. The behaviors recorded were: resting in water, resting hauled out, maintenance, breeding display, breeding behavior, aggression, pattern swimming, random swimming, exploration, and out of sight. Activity levels (random swimming and exploration) were expected to increase, while stereotypic behaviors (pattern swimming) were expected to decrease. The frequency and duration of behaviors were documented for 90 hr in both the control phase (without enrichment) and the experimental phase (with enrichment). Statistically significant differences (P<0.05) in the time spent in pattern swimming, random swimming, exploration, and out of sight were observed between the two phases. With enrichment, pattern swimming and out of sight decreased, while random swimming and exploration behavior increased. These findings demonstrate that enrichment can promote behaviors (random swimming and exploration) that are likely to be normal for phocids in the wild, and that may contribute to the behavioral complexity of these seals in captivity. Zoo Biol 21:375–387, 2002. © 2002 Wiley‐Liss, Inc.     

Molecular methods for differentiating grey seal (Halichoerus grypus) and harbour seal (Phoca vitulina) scat

Pinniped dietary information is crucial for understanding marine ecosystems; however, in the North Atlantic, grey and harbour seals haulout concomitantly and their faeces are visually indistinguishable. Therefore, we developed molecular methods to differentiate the species' scat. PCR primers were created that amplify a portion of mitochondrial 16S ribosomal DNA in grey and harbour seals. The samples were amplified and the resulting products were digested using the restriction enzyme Tsp509I, producing diagnostic banding patterns. These tools provide a mechanism by which separate dietary analysis can be achieved for grey and harbour seals at mixed haulouts in New England.     

Satellite tracking of grey seals (Halichoerus grypus)

Three types of Argos satellite transmitter were attached to grey seals ( Halichoerus grypus ) at Donna Nook (South Humberside, UK) between 1985 and 1989 in order to investigate their movements. With the first two transmitters (A and B) the entire package was attached to the seal's back. Seal A was tracked for 29 days but although it was located on sandbanks up to 150 km south-east of Donna Nook, no locations were obtained at sea. Transmitters B and C used a submergence sensor to regulate transmissions. Seal B was tracked for 51 days and remained within 40 km of Donna Nook. A few locations were obtained at sea but all within 10 km of Donna Nook. Transmitter C incorporated a head-mounted aerial in order to increase the number of location fixes when the seal was at sea. This seal was tracked for 111 days, producing an average of 9·1 location fixes per day while at sea. It used two sites 265 km apart and undertook three transits between them. On the second visit to the northern site it made several trips up to 55 km out to sea. The majority of the remainder of the time was spent within 10 km of the haulout sites. Estimates of swimming speed were consistent with values required for minimum cost of transport.     

Mycoplasma phocidae sp. nov., isolated from harbor seals (Phoca vitulina L.).

In 1979 and 1980, more than 400 harbor seals (Phoca vitulina) along the New England coast of the United States died of epizootic pneumonia that was attributed to an influenza virus. Six mycoplasma isolates that were recovered from the respiratory tracts of affected seals were investigated and were found to be serologically identical and distinct from previously described species. These isolates required serum for growth, did not possess a cell wall, and did not hydrolyze urea. Arginine was hydrolyzed, glucose was not fermented, film and spots were observed on horse serum agar, phosphatase was produced, tetrazolium was not reduced, and serum and casein were not digested. The guanine-plus-cytosine content of the DNA was 27.8 mol%. We propose the name Mycoplasma phocidae for these isolates. The type strain of M. phocidae is strain 105 (= ATCC 33657).     

Experimental Toxoplasma gondii infection in grey seals (Halichoerus grypus)

Laboratory-reared animals were used to assess the susceptibility of seals (Halichoerus grypus) to Toxoplasma gondii infection. Four seals were each orally inoculated with 100 or 10,000 oocysts of T. gondii (VEG strain), and another 4 seals served as negative controls. Occasionally, mild behavioral changes were observed in all inoculated seals but not in control animals. A modified agglutination test revealed the presence of antibodies to T. gondii in sera collected from inoculated seals and mice inoculated as controls. No evidence of the parasite was found on an extensive histological examination of seal tissues, and immunohistochemical staining of tissue sections from inoculated seals revealed a single tissue cyst in only 1 seal. Control mice inoculated with 10 oocysts from the same inoculum given to seals became serologically and histologically positive for T. gondii. Cats that were fed brain or muscle tissue collected from inoculated seals passed T. gondii oocysts in feces. This study demonstrates that T. gondii oocysts can establish viable infection in seals and supports the hypothesis that toxoplasmosis in marine mammals can be acquired from oocysts in surface water runoff and sewer discharge.     

Trophic niche overlap between sympatric harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus) at the southern limit of their European range (Eastern English Channel)

Sympatric harbour (Phoca vitulina) and grey seals (Halichoerus grypus) are increasingly considered potential competitors, especially since recent local declines in harbour seal numbers while grey seal numbers remained stable or increased at their European core distributions. A better understanding of the interactions between these species is critical for conservation efforts. This study aimed to identify the trophic niche overlap between harbour and grey seals at the southern limit of their European range, in the Baie de Somme (BDS, Eastern English Channel, France), where numbers of resident harbour seals and visiting grey seals are increasing exponentially. Dietary overlap was identified from scat contents using hierarchical clustering. Isotopic niche overlap was quantified using δ¹³C and δ¹⁵N isotopic values from whiskers of 18 individuals, by estimating isotopic standard ellipses with a novel hierarchical model developed in a Bayesian framework to consider both intraindividual variability and interindividual variability. Foraging areas of these individuals were identified from telemetry data. The three independent approaches provided converging results, revealing a high trophic niche overlap due to consumption of benthic flatfish. Two diet clusters were dominated by either small or large benthic flatfish; these comprised 85.5% [CI95%: 80.3%–90.2%] of harbour seal scats and 46.8% [35.1%–58.4%] of grey seal scats. The narrower isotopic niche of harbour seals was nested within that of grey seals (58.2% [22.7%–100%] overlap). Grey seals with isotopic values similar to harbour seals foraged in coastal waters close to the BDS alike harbour seals did, suggesting the niche overlap may be due to individual grey seal strategies. Our findings therefore provide the basis for potential competition between both species (foraging on benthic flatfish close to the BDS). We suggest that a continued increase in seal numbers and/or a decrease in flatfish supply in this area could cause/amplify competitive interactions and have deleterious effects on harbour seal colonies.     

Movements, diving and foraging behaviour of grey seals (Halichoerus grypus)

This study presents the first direct observations of the movements and behaviour of free-ranging grey seals at sea. Radio and ultrasonic transmitters were attached to three sub-adult male grey seals which were then tracked from a suitable vessel. Behaviour at sea fell into one of three categories: travelling between haul-outs, short duration trips, and resting adjacent to haul-out sites. Travelling was characterized by direct, relatively fast horizontal movement and by V-shaped dive profiles. During short duration trips the seals swam slower and invariably exhibited square-wave dive profiles, spending approximately 60% of total dive duration at the maximum depth. Resting involved shallow dives close to haul-out sites and an absence of directed lateral movement.
The excellent navigational abilities of grey seals are illustrated by the rapid, direct swimming between distant haul-out sites. It is proposed that short duration trips are specifically for foraging because of their association with other piscivores, and because swimming was slow and mostly on or near the sea bed (grey seals are known to feed almost exclusively on demersal and benthic fish). These trips accounted for only 14% of the nine days that seal 1 was tracked. It is also proposed that the habit of diving to the sea bed whilst travelling between distant haul-out sites is to allow opportunistic foraging with only a small increase in total swimming distance.     

Sealpox in captive grey seals (Halichoerus grypus) and their handlers

Histopathologic, ultrastructural, and negative-staining studies indicated that nodular lesions on the flippers, head, and necks of recently weaned, captive grey seals (Halichoerus grypus) were similar to sealpox lesions reported from several other species of seals. Virions associated with the nodules were characteristic of the parapoxvirus subgroup of pox viruses. Two of the three persons handling the seals developed nodular lesions similar to "milker's nodules," the characteristic lesion in persons infected with parapoxvirus. The clinical course of the parapoxvirus infection in both the grey seals and their handlers is described. It was concluded that although sealpox is transmissible to man, the mild clinical manifestations place it in the nuisance category of zoonotic diseases.     

Finding fathers: spatio-temporal analysis of paternity assignment in grey seals (Halichoerus grypus)

Molecular studies of pinniped breeding systems exhibit a broad range of agreement and disagreement with observational indices of male breeding success. Grey seal studies have reported considerable discrepancies between genetic and behavioural paternity measures that have been interpreted as evidence of previously unidentified male strategies and/or tactics. Therefore, these studies have the power to fundamentally alter our perceptions of mating systems. However, other pinniped studies exhibit no such disagreements, and one possible explanation for disparities may be sampling biases in space and time. Therefore, it is essential that potential sampling biases are examined to evaluate the likelihood of previously unidentified male strategies. We examined paternities assigned at the North Rona grey seal colony between 1999 and 2002 in relation to concurrent detailed behavioural and locational data for males and females. We found that (i) for females observed in sexual interaction(s) during their oestrus period, it was highly probable that one of the interacting males fathered their next pup; (ii) over 80% of assigned paternities agreed with observations of the in-colony behaviour and spatio-temporal proximity of the males and females involved; and (iii) a minority of females exhibit mate choice and seek sires outside their local male's home range, although evidence suggests that these females mate on the colony rather than at sea. In conclusion, nearly all paternities assigned agreed with expectation based upon detailed knowledge of the spatio-temporal patterns of individuals during the breeding season. We found little evidence of unidentified male strategies at North Rona, Scotland, whereas further examination of mechanisms of female choice may be productive.     

Play in Harbour seals (Phoca vitulina)

Harbour seals in a breeding colony at Miquelon exhibited 13 distinct types of play behaviour, 80% of which was solitary locomotor play. Most play was displayed by yearlings and juveniles, though a significant amount of adult play occurred as well. Mothers and pups rarely played. Yearlings played socially as often as alone, but seals of other age classes played by themselves most often. Only social play resembled adult activities. It is suggested that the function of mammalian play has been obscured by its similarity to adult behaviour.     

The occurrence of myocardial bridges on coronary arteries in the common seal (Phoca vitulina vitulina)

Myocardial bridging in the common seal (Phoca vitulina vitulina) has been described in 4 hearts. In a collection of 40 hearts 10 cases(20%) were present. In most of the hearts the vessels in the sulcus interventricularis subsinuosus are overbridged.     

Geographic variation of the major histocompatibility complex in Eastern Atlantic grey seals (Halichoerus grypus)

Pathogen-driven balancing selection maintains high genetic diversity in many vertebrates, particularly in the major histocompatibility complex (MHC) immune system gene family, which is often associated with disease susceptibility. In large natural populations where subpopulations face different pathogen pressures, the MHC should show greater genetic differentiation within a species than neutral markers. We examined genetic diversity at the MHC-DQB locus and nine putatively neutral microsatellite markers in grey seals (Halichoerus grypus) from eight United Kingdom (UK) colonies, the Faeroe Islands and Sable Island, Canada. Five DQB alleles were identified in grey seals, which varied in prevalence across the grey seal range. Among the seal colonies, significant differences in DQB allele and haplotype frequencies and in average DQB heterozygosity were observed. Additionally, the DQB gene exhibited greater differentiation among colonies compared with neutral markers, yet a weaker pattern of isolation by distance (IBD). After correcting for the underlying IBD pattern, subpopulations breeding in similar habitats were more similar to one another in DQB allele frequencies than populations breeding in different habitats, but the same did not hold true for microsatellites, suggesting that habitat-specific pathogen pressure influences MHC evolution. Overall, the data are consistent with selection at MHC-DQB loci in grey seals with both varying selective pressures and geographic population structure appearing to influence the DQB genetic composition of breeding colonies.     

Dispersion and site fidelity of breeding female grey seals (Halichoerus grypus) on North Rona, Scotland

Female grey seals ( Halichoerus grypus ) formed breeding aggregations on the island of North Rona, Scotland. Aggregations of females were associated particularly with gullies leading from the sea, leaving large areas of available space unoccupied. Changes in the degree of aggregation of females during the breeding season were similar in 1987, 1988 and 1989. Pronounced aggregations occurred in the early and late parts of each breeding season.
Of 67 breeding females marked in 1985, 62 (93%)) returned to N. Rona to breed in at least one season up to 1989, but 18 (27%) were present in all five years. Females came ashore up to 14 days before giving birth and 82% were observed first in the vicinity of their subsequent pupping site. Between 1985 and 1989, marked females which returned were faithful to their previous pupping sites, even when the previous pup had died. There was no evidence of a gradual change in the location of individual pupping sites over time. This pupping site fidelity may generate aggregations whose location, timing and composition is predictable.     

Finescale topographical correlates of behavioural investment in offspring by female grey seals, Halichoerus grypus

Grey seals breed colonially on substrates ranging from ice to rocky or sandy beaches. Clear differences in seal behaviour patterns exist among such broad classes of breeding habitat. However, finer scale topographical variation is likely to influence individual behaviour with consequences for pupping success. We examined topographical influences on the behaviour of breeding female grey seals by quantifying topography at a subseal size resolution. Using submetre resolution digital terrain models of two sites within a rocky breeding colony, we compared site topography in relation to observed differences in female behaviour at these sites. Females at both sites preferred breeding close to water (standing pools or sea) and frequently commuted between their pups and water. Topographical models indicated that one site was more costly for seals in terms of their locations and movements within the site. This was due to a lack of low-elevation land adjacent to the main access points from the sea and the reduced availability of pools. Females at this site showed reduced pup attendance and an increase in energetically costly behaviours, whilst females at the lower-cost site spent more time interacting with their pups and resting. These topographically induced behavioural differences are likely to affect the quantity and quality of pup provisioning by mothers and influence individual pupping site selection. Less costly sites are likely to be colonized preferentially and by larger, older and more dominant females, potentially generating finescale spatial heterogeneity in female quality within the breeding colony. Copyright 2000 The Association for the Study of Animal Behaviour.     

Genetic association with boldness and maternal performance in a free-ranging population of grey seals (Halichoerus grypus)

Individual variation in quantitative traits clearly influence many ecological and evolutionary processes. Moderate to high heritability estimates of personality and life-history traits suggest some level of genetic control over these traits. Yet, we know very little of the underlying genetic architecture of phenotypic variation in the wild. In this study, we used a candidate gene approach to investigate the association of genetic variants with repeated measures of boldness and maternal performance traits (weaning mass and lactation duration) collected over an 11- and 28-year period, respectively, in a free-ranging population of grey seals on Sable Island National Park Reserve, Canada. We isolated and re-sequenced five genes: dopamine receptor D4 (DRD4), serotonin transporter (SERT), oxytocin receptor (OXTR), and melanocortin receptors 1 (MC1R) and 5 (MC5R). We discovered single nucleotide polymorphisms (SNPs) in each gene; and, after accounting for loci in linkage disequilibrium and filtering due to missing data, we were able to test for genotype-phenotype relationships at seven loci in three genes (DRD4, SERT, and MC1R). We tested for association between these loci and traits of 180 females having extreme shy-bold phenotypes using mixed-effects models. One locus within SERT was significantly associated with boldness (effect size = 0.189) and a second locus within DRD4 with weaning mass (effect size = 0.232). Altogether, genotypes explained 6.52–13.66% of total trait variation. Our study substantiates SERT and DRD4 as important determinants of behaviour, and provides unique insight into the molecular mechanisms underlying maternal performance variation in a marine predator.Subject terms: Behavioural ecology, Evolutionary genetics, Behavioural genetics, Genetic association study, Quantitative trait