Classifying grey seal behaviour in relation to environmental variability and commercial fishing activity - a multivariate hidden Markov model.

Classifying movement behaviour of marine predators in relation to anthropogenic activity and environmental conditions is important to guide marine conservation. We studied the relationship between grey seal (Halichoerus grypus) behaviour and environmental variability in the southwestern Baltic Sea where seal-fishery conflicts are increasing. We used multiple environmental covariates and proximity to active fishing nets within a multivariate hidden Markov model (HMM) to quantify changes in movement behaviour of grey seals while at sea. Dive depth, dive duration, surface duration, horizontal displacement, and turning angle were used to identify travelling, resting and foraging states. The likelihood of seals foraging increased in deeper, colder, more saline waters, which are sites with increased primary productivity and possibly prey densities. Proximity to active fishing net also had a pronounced effect on state occupancy. The probability of seals foraging was highest <5 km from active fishing nets (51%) and decreased as distance to nets increased. However, seals used sites <5 km from active fishing nets only 3% of their time at sea highlighting an important temporal dimension in seal-fishery interactions. By coupling high-resolution oceanographic, fisheries, and grey seal movement data, our study provides a scientific basis for designing management strategies that satisfy ecological and socioeconomic demands on marine ecosystems.

Hawaiian monk seals exhibit behavioral flexibility when targeting prey of different size and shape.

Animals use diverse feeding strategies to capture and consume prey, with many species switching between strategies to accommodate different prey. Many marine animals exhibit behavioral flexibility when feeding to deal with spatial and temporal heterogeneity in prey resources. However, little is known about flexibility in the feeding behavior of many large marine predators. Here, we documented the feeding behavior and kinematics of the endangered Hawaiian monk seal (Neomonachus schauinslandi, n=7) through controlled feeding trials. Seals were fed multiple prey types (e.g. night smelt, capelin, squid and herring) that varied in size and shape to examine behavioral flexibility in feeding. Hawaiian monk seals primarily used suction feeding (91% of all feeding trials) across all prey types, but biting, specifically pierce feeding, was also observed (9% of all feeding trials). Suction feeding was characterized by shorter temporal events, a smaller maximum gape and gape angle, and a fewer number of jaw motions than pierce feeding; suction feeding kinematic performance was also more variable compared with pierce feeding. Seals showed behavioral flexibility in their use of the two strategies. Suction feeding was used most frequently when targeting small to medium sized prey and biting was used with increasing frequency on larger prey. The feeding kinematics differed between feeding strategies and prey types, showing that Hawaiian monk seals adjusted their behaviors to particular feeding contexts. Hawaiian monk seals are opportunistic marine predators and their ability to adapt their feeding strategy and behavior to specific foraging scenarios allows them to target diverse prey resources.

Underwater vocal complexity of Arctic seal Erignathus barbatus in Kongsfjorden (Svalbard).

In this study the description of underwater vocal repertoire of bearded seal in Svalbard (Norway) was extended. Two autonomous passive acoustic recorders were deployed for one year (August 2014-July 2015) in the inner and outer parts of the Kongsfjorden, and 1728 h were recorded and 17 220 vocalizations were found. Nine different vocalization classes were identified and characterized using ten acoustic parameters. The calls showed heterogeneous spectral features, but share the descending trend of frequency modulation. The different classes emerged were discriminated primarily by bandwidth and duration, and then by minimum frequency, central frequency, and maximum frequency in this order. This study represents a step forward to improve the understanding of the acoustic behaviour and the social function of these calls, and identified long passive acoustic monitoring as an effective method to assess vocal complexity and the ecology of marine species producing sounds.

Variability in sea ice cover and climate elicit sex specific responses in an Antarctic predator.

Contrasting regional changes in Southern Ocean sea ice have occurred over the last 30 years with distinct regional effects on ecosystem structure and function. Quantifying how Antarctic predators respond to such changes provides the context for predicting how climate variability/change will affect these assemblages into the future. Over an 11-year time-series, we examine how inter-annual variability in sea ice concentration and advance affect the foraging behaviour of a top Antarctic predator, the southern elephant seal. Females foraged longer in pack ice in years with greatest sea ice concentration and earliest sea ice advance, while males foraged longer in polynyas in years of lowest sea ice concentration. There was a positive relationship between near-surface meridional wind anomalies and female foraging effort, but not for males. This study reveals the complexities of foraging responses to climate forcing by a poleward migratory predator through varying sea ice property and dynamic anomalies.

Maternal Oxytocin Is Linked to Close Mother-Infant Proximity in Grey Seals (Halichoerus grypus).

Maternal behaviour is a crucial component of reproduction in all mammals; however the quality of care that mothers give to infants can vary greatly. It is vital to document variation in maternal behaviour caused by the physiological processes controlling its expression. This underlying physiology should be conserved throughout reproductive events and should be replicated across all individuals of a species; therefore, any correlates to maternal care quality may be present across many individuals or contexts. Oxytocin modulates the initiation and expression of maternal behaviour in mammals; therefore we tested whether maternal plasma oxytocin concentrations correlated to key maternal behaviours in wild grey seals (Halichoerus grypus). Plasma oxytocin concentrations in non-breeding individuals (4.3 ± 0.5 pg/ml) were significantly lower than those in mothers with dependent pups in both early (8.2 ± 0.8 pg/ml) and late (6.9 ± 0.7 pg/ml) lactation. Maternal plasma oxytocin concentrations were not correlated to the amount of nursing prior to sampling, or a mother's nursing intensity throughout the dependent period. Mothers with high plasma oxytocin concentrations stayed closer to their pups, reducing the likelihood of mother-pup separation during lactation which is credited with causing starvation, the largest cause of pup mortality in grey seals. This is the first study to link endogenous oxytocin concentrations in wild mammalian mothers with any type of maternal behaviour. Oxytocin's structure and function is widely conserved across mammalian mothers, including humans. Defining the impact the oxytocin system has on maternal behaviour highlights relationships that may occur across many individuals or species, and such behaviours heavily influence infant development and an individual's lifetime reproductive success.

Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities.

Adult Weddell seals (Leptonychotes weddellii) haul-out on the ice in October/November (austral spring) for the breeding season and reduce foraging activities for ~4 months until their molt in the austral fall (January/February). After these periods, animals are at their leanest and resume actively foraging for the austral winter. In mammals, decreased exercise and hypoxia exposure typically lead to decreased production of O2-carrying proteins and muscle wasting, while endurance training increases aerobic potential. To test whether similar effects were present in marine mammals, this study compared the physiology of 53 post-molt female Weddell seals in the austral fall to 47 pre-breeding females during the spring in McMurdo Sound, Antarctica. Once body mass and condition (lipid) were controlled for, there were no seasonal changes in total body oxygen (TBO2) stores. Within each season, hematocrit and hemoglobin values were negatively correlated with animal size, and larger animals had lower mass-specific TBO2 stores. But because larger seals had lower mass-specific metabolic rates, their calculated aerobic dive limit was similar to smaller seals. Indicators of muscular efficiency, myosin heavy chain composition, myoglobin concentrations, and aerobic enzyme activities (citrate synthase and ß-hydroxyacyl CoA dehydrogenase) were likewise maintained across the year. The preservation of aerobic capacity is likely critical to foraging capabilities, so that following the molt Weddell seals can rapidly regain body mass at the start of winter foraging. In contrast, muscle lactate dehydrogenase activity, a marker of anaerobic metabolism, exhibited seasonal plasticity in this diving top predator and was lowest after the summer period of reduced activity.

Prolonged food deprivation increases mRNA expression of deiodinase 1 and 2, and thyroid hormone receptor ß-1 in a fasting-adapted mammal.

Food deprivation in mammals is typically associated with reduced thyroid hormone (TH) concentrations and deiodinase content and activity to suppress metabolism. However, in prolonged-fasted, metabolically active elephant seal pups, TH levels are maintained, if not elevated. The functional relevance of this apparent paradox is unknown and demonstrates variability in the regulation of TH levels, metabolism and function in food-deprived mammals. To address our hypothesis that cellular TH-mediated activity is upregulated with fasting duration, we quantified the mRNA expression and protein content of adipose and muscle deiodinase type I (DI1) and type II (DI2), and TH receptor beta-1 (THrß-1) after 1, 3 and 7 weeks of fasting in northern elephant seal pups (N=5-7 per week). Fasting did not decrease the concentrations of plasma thyroid stimulating hormone, total triiodothyronine (tT3), free T3, total thyroxine (tT4) or free T4, suggesting that the hypothalamic-pituitary-thyroid axis is not suppressed, but rather maintained during fasting. Mean mRNA expression of adipose DI1 and DI2 increased threefold and fourfold, respectively, and 20- and 30-fold, respectively, in muscle. With the exception of adipose DI1, protein expression of adipose DI2 and muscle DI1 and DI2 increased twofold to fourfold. Fasting also increased adipose (fivefold) and muscle (fourfold) THrß-1 mRNA expression, suggesting that the mechanisms mediating cellular TH activity are upregulated with prolonged fasting. The data demonstrate a unique, atypical mechanism of TH activity and regulation in mammals adapted to prolonged food deprivation in which the potential responsiveness of peripheral tissues and cellular TH activity are increased, which may contribute to their lipid-based metabolism.

Hydrodynamic perception in true seals (Phocidae) and eared seals (Otariidae).

Pinnipeds, that is true seals (Phocidae), eared seals (Otariidae), and walruses (Odobenidae), possess highly developed vibrissal systems for mechanoreception. They can use their vibrissae to detect and discriminate objects by direct touch. At least in Phocidae and Otariidae, the vibrissae can also be used to detect and analyse water movements. Here, we review what is known about this ability, known as hydrodynamic perception, in pinnipeds. Hydrodynamic perception in pinnipeds developed convergently to the hydrodynamic perception with the lateral line system in fish and the sensory hairs in crustaceans. So far two species of pinnipeds, the harbour seal (Phoca vitulina) representing the Phocidae and the California sea lion (Zalophus californianus) representing the Otariidae, have been studied for their ability to detect local water movements (dipole stimuli) and to follow hydrodynamic trails, that is the water movements left behind by objects that have passed by at an earlier point in time. Both species are highly sensitive to dipole stimuli and can follow hydrodynamic trails accurately. In the individuals tested, California sea lions were clearly more sensitive to dipole stimuli than harbour seals, and harbour seals showed a superior trail following ability as compared to California sea lions. Harbour seals have also been shown to derive additional information from hydrodynamic trails, such as motion direction, size and shape of the object that caused the trail (California sea lions have not yet been tested). The peculiar undulated shape of the harbour seals' vibrissae appears to play a crucial role in trail following, as it suppresses self-generated noise while the animal is swimming.

The effects of handling and anesthetic agents on the stress response and carbohydrate metabolism in northern elephant seals.

Free-ranging animals often cope with fluctuating environmental conditions such as weather, food availability, predation risk, the requirements of breeding, and the influence of anthropogenic factors. Consequently, researchers are increasingly measuring stress markers, especially glucocorticoids, to understand stress, disturbance, and population health. Studying free-ranging animals, however, comes with numerous difficulties posed by environmental conditions and the particular characteristics of study species. Performing measurements under either physical restraint or chemical sedation may affect the physiological variable under investigation and lead to values that may not reflect the standard functional state of the animal. This study measured the stress response resulting from different handling conditions in northern elephant seals and any ensuing influences on carbohydrate metabolism. Endogenous glucose production (EGP) was measured using [6-(3)H]glucose and plasma cortisol concentration was measured from blood samples drawn during three-hour measurement intervals. These measurements were conducted in weanlings and yearlings with and without the use of chemical sedatives--under chemical sedation, physical restraint, or unrestrained. We compared these findings with measurements in adult seals sedated in the field. The method of handling had a significant influence on the stress response and carbohydrate metabolism. Physically restrained weanlings and yearlings transported to the lab had increased concentrations of circulating cortisol (F(11, 46) = 25.2, p<0.01) and epinephrine (F(3, 12) = 5.8, p = 0.01). Physical restraint led to increased EGP (t = 3.1, p = 0.04) and elevated plasma glucose levels (t = 8.2, p<0.01). Animals chemically sedated in the field typically did not exhibit a cortisol stress response. The combination of anesthetic agents (Telazol, ketamine, and diazepam) used in this study appeared to alleviate a cortisol stress response due to handling in the field without altering carbohydrate metabolism. Measures of hormone concentrations and metabolism made under these conditions are more likely to reflect basal values.

Do male northern elephant seals recognize individuals or merely relative dominance rank?

Vocal recognition was tested in a socially dynamic context where many individuals interact: the female defense polygyny practiced by male northern elephant seals. The goal was to tease apart whether animals recognize other individuals or instead use a simple rule-based category (i.e., relative dominance rank). A total of 67 playback experiments conducted with 18 males at Año Nuevo State Reserve, California, tested three aspects of recognition: (1) recognition of relative rank; (2) whether such recognition was continuous or categorical; and (3) recognition of familiarity. Results indicate that males recognize familiar individuals although responses are primarily based on relative dominance rank.

In situ measures of foraging success and prey encounter reveal marine habitat-dependent search strategies.

Predators are thought to reduce travel speed and increase turning rate in areas where resources are relatively more abundant, a behavior termed "area-restricted search." However, evidence for this is rare, and few empirical data exist for large predators. Animals exhibiting foraging site fidelity could also be spatially aware of suitable feeding areas based on prior experience; changes in movement patterns might therefore arise from the anticipation of higher prey density. We tested the hypothesis that regions of area-restricted search were associated with a higher number of daily speed spikes (a proxy for potential prey encounter rate) and foraging success in southern elephant seals (Mirounga leonina), a species exhibiting both area-restricted searches and high interannual foraging site fidelity. We used onshore morphological measurements and diving data from archival tags deployed during winter foraging trips. Foraging success was inferred from in situ changes in relative lipid content derived from measured changes in buoyancy, and first-passage time analysis was used to identify area-restricted search behavior. Seals exhibited relatively direct southerly movement on average, with intensive search behavior predominantly located at the distal end of tracks. The probability of being in search mode was positively related to changes in relative lipid content; thus, intensively searched areas were associated with the highest foraging success. However, there was high foraging success during the outward transit even though seals moved through quickly without slowing down and increasing turning rate to exploit these areas. In addition, the probability of being in search mode was negatively related to the number of daily speed spikes. These results suggest that movement patterns represent a response to prior expectation of the location of predictable and profitable resources. Shelf habitat was 4-9 times more profitable than the other habitats, emphasizing the importance of the East Antarctic shelf for this and other predators in the region. We have provided rare empirical data with which to investigate the relationship between predator foraging strategy and prey encounter/ foraging success, underlining the importance of inferring the timing and spatial arrangement of successful food acquisition for interpreting foraging strategies correctly.

The influence of behavioural context on Weddell seal (Leptonychotes weddellii) airborne mother-pup vocalisation.

Previous mammalian studies have demonstrated that varying levels of signaller arousal are frequently expressed through vocal behaviour. The potential for callers to convey their motivational state may ensure that recipient responses are appropriate to their needs. The current study investigated the influence of behavioural context on Weddell seal mother-pup vocalisation. Mother and pup call rates were calculated within five and seven behavioural contexts, respectively, and the acoustic characteristics of 69 pup calls were measured within four contexts (total calls = 276). Context significantly influenced the temporal patterning of calls, with reuniting mothers and pups and lone active pups emitting more calls than during mother-pup contact periods. Reuniting and lone pup calls were also characterised by longer durations, higher fundamental frequencies, and increased energy in upper harmonics. Results suggest that reunion events and lone pup searching are characterised by calls reflective of heightened arousal, compared with mother-pup contact periods.

Aversiveness of sounds in phocid seals: psycho-physiological factors, learning processes and motivation.

Aversiveness of sounds and its underlying physiological mechanisms in mammals are poorly understood. In this study we tested the influence of psychophysical parameters, motivation and learning processes on the aversiveness of anthropogenic underwater noise in phocid seals (Halichoerus grypus and Phoca vitulina). We compared behavioural responses of seals to playbacks of sounds based on a model of sensory unpleasantness for humans, sounds from acoustic deterrent devices and sounds with assumed neutral properties in different contexts of food motivation. In a captive experiment with food presentation, seals habituated quickly to all sound types presented at normalised received levels of 146 dB re. 1 microPa (r.m.s., root mean square). However, the fast habituation of avoidance behaviour was also accompanied by a weak sensitisation process affecting dive times and place preference in the pool. Experiments in the wild testing animals without food presentation revealed differential responses of seals to different sound types. We observed avoidance behaviour at received levels of 135-144 dB re. 1 microPa (sensation levels of 59-79 dB). In this experiment, sounds maximised for 'roughness' perceived as unpleasant by humans also caused the strongest avoidance responses in seals, suggesting that sensory pleasantness may be the result of auditory processing that is not restricted to humans. Our results highlight the importance of considering the effects of acoustic parameters other than the received level as well as animal motivation and previous experience when assessing the impacts of anthropogenic noise on animals.

The impact of climatic variation on the opportunity for sexual selection.

Many studies have demonstrated influences of climatic variation on a variety of ecological processes, however, its impact on the potent evolutionary force of sexual selection has largely been ignored. The intensity of sexual selection is a fundamental parameter in animal populations, which depends upon the degree of polygamy and will probably be influenced by the impact of local climatic variation upon 'environmental potential for polygamy'. Here, we provide evidence of a direct effect of local climatic variation on the intensity of sexual selection, by showing a clear correlation between local weather conditions and inter-annual changes in the degree of polygamy in a long-term study of colonially breeding grey seals (Halichoerus grypus). Our results show that changes in local weather conditions alter the annual proportion of males contributing to the effective population size (Ne) by up to 61%. Consequently, over the 'lifetime' of a cohort, a broader range of individuals will contribute genetically to the next generation if local weather conditions are variable. In the context of predicted future changes in climatic variation, these findings have broad implications for population genetics of socially structured animal systems through the major influence that the degree of polygamy has upon Ne.

Physiology and behavior influence lactation efficiency in northern elephant seals (Mirounga angustirostris).

The efficiency with which mothers convert acquired energy into milk is a key determinant of the magnitude of parental investment in mammals; however, the mechanisms underlying lactation efficiency are poorly understood. Investigations on northern elephant seals have shown lactation efficiency, measured as the proportion of total energy expenditure that goes to the pup as milk, increases with age. In a cross-sectional study the physiological and behavioral determinants of lactation efficiency were investigated in eight young and seven prime (older) elephant seals by conducting behavioral observations and collecting milk, blood, and tissue on days 3 and 22 of lactation. Milk composition, circulating fatty acid and triglyceride concentrations, and mammary and blubber lipoprotein lipase activity were determined. Prime females had significantly greater percent milk fat and circulating fatty acids on day 3 than did young females, but these differences disappeared by day 22. The ability for prime females to produce higher-energy milk early in lactation may allow them to increase lactation efficiency by increasing the rate of energy transfer. In addition, prime females spent significantly more time resting. A combination of reduced activity and more rapid energy delivery likely explains the increase in lactation efficiency with age found in a previous study.

Patterns in the vocalizations of male harbor seals.

Comparative analyses of the roar vocalization of male harbor seals from ten sites throughout their distribution showed that vocal variation occurs at the oceanic, regional, population, and subpopulation level. Genetic barriers based on the physical distance between harbor seal populations present a likely explanation for some of the observed vocal variation. However, site-specific vocal variations were present between genetically mixed subpopulations in California. A tree-based classification analysis grouped Scottish populations together with eastern Pacific sites, rather than amongst Atlantic sites as would be expected if variation was based purely on genetics. Lastly, within the classification tree no individual vocal parameter was consistently responsible for consecutive splits between geographic sites. Combined, these factors suggest that site-specific variation influences the development of vocal structure in harbor seals and these factors may provide evidence for the occurrence of vocal dialects.

Patterns of paternal relatedness in British grey seal colonies.

Previous studies of breeding behaviour in the grey seal, Halichoerus grypus, have painted conflicting pictures. Behavioural observations suggest a classical polygynous system with a small number of dominant males fathering most of the offspring. However, genetic analysis suggests that many potential fathers spend little time ashore, that some pairs of seals show partner fidelity and that the dominant males are not as successful as their behaviour would suggest. Here we used paternal relatedness between pups with known mothers, sampled over an 11-year period, to show that behavioural dominance leading to enhanced fitness is a feature of only a handful of males located near the centre of the breeding colony. The vast majority of pups are fathered by any of a large number of males who all share approximately equal success, including virtually all those males who have previously escaped our best sampling efforts. As expected, the frequency of full-sibs is reduced in this longer time series relative to the original study. However, absolute estimates of the frequency of full-sibs seem to be confounded by a tendency for females who produce paternally unrelated pups to have conceived to males who are more genetically dissimilar from each other than expected by chance alone. Together, these elements of breeding behaviour would help to maintain maximum genetic diversity and to minimize the effects of inbreeding.

Salinity discrimination in harbour seals: a sensory basis for spatial orientation in the marine environment?

Salinity variations can be considered as a potential source of information for orientation in the marine environment. To use this kind of environmental information marine animals must be able to detect these salinity differences. Therefore we determined salinity-difference thresholds of two harbour seals for the discrimination of seawater solutions as a function of the salinity level (15-35@1000) and compared them with the thresholds of human subjects. Whereas in humans thresholds increased with increasing salinity level, thresholds of seals decreased with increasing salinity level. Both seals achieved best sensitivity at 30/1000 salinity, where they detected a salinity difference < or = 4%. These data indicate that the ability of seals to detect salinity differences of seawater is well tuned to the natural occurrence of this environmental information. Their high gustatory resolving power for differences in seawater salinity is suggested to meet the basic requirements for chemosensory orientation of seals in the marine habitat.