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Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction.

Human-induced changes to natural systems can cause major disturbances to fundamental ecological and population processes and result in local extinctions and secondary contacts between formerly isolated species. Extensive fur seal harvesting during the nineteenth century on Macquarie Island (subantarctic) resulted in extinction of the original population. Recolonization by three species has been slow and complex, characterized by the establishment of breeding groups of Antarctic and subantarctic fur seals (Arctocephalus gazella and Arctocephalus tropicalis) and presumed nonbreeding (itinerant) male New Zealand fur seals (Arctocephalus forsteri). One thousand and seven pups from eight annual cohorts (1992-2003) were analysed using mitochondrial control region data (RFLP) and 10 microsatellite loci to estimate species composition and hybridization. Antarctic fur seals predominated, but hybridization occurred between all three species (17-30% of all pups). Involvement of New Zealand fur seals was unexpected as females are absent and males are not observed to hold territories during the breeding season. The proportion of hybrids in the population has fallen over time, apparently owing to substantial influxes of pure Antarctic and subantarctic individuals and non-random mating. Over 50% of New Zealand hybrids and 43% of Antarctic-subantarctic hybrids were not F(1), which indicates some degree of hybrid reproductive success, and this may be underestimated: simulations showed that hybrids become virtually undetectable by the third generation of backcrossing. While human impacts seem to have driven novel hybridization in this population, the present 'time slices' analysis suggests some biological resistance to complete homogenization.

Alleles↗

Nasal heat and water exchange is not an effector mechanism for water balance regulation in grey seals.

Phocid seals may effectively restrict respiratory heat and water loss by nasal heat and water exchange (NHE), and respiratory heat loss is, in fact, subject to thermoregulatory control. We have investigated whether phocid seals also control NHE and respiratory water loss to regulate water balance. Three resting juvenile female grey seals (Halichoerus grypus) were subjected to: (i) 5 days of food and water deprivation, (ii) intravenous infusion of 1000 ml of a hypersomotic (930 mM) solution of the diuretic mannitol, and (iii) oral injection of 1500 ml distilled water. During these experiments in air of 0 degree C, expired air temperature (T(ex)) and respiratory frequency (f) were recorded, and urine and blood samples collected. The results were compared with results from control experiments. Five days of food and water deprivation caused an average 10.5% and 20.8% increase in plasma (PO) and urine (UO) osmolality, respectively. Mannitol infusion induced excessive diuresis and caused an average 2.45% reduction of the estimated body water pool. Water loading caused an average 4.5% and 60% reduction in PO and UO, respectively, while urine production increased by 365%, on average. However, in no case did either T(ex) or f change significantly from mean control levels of 22.4 (range: 20.7-25.2) degrees C and 7.3 (range: 6.6-8.4) breaths min-1, respectively. Thus, water balance disturbances that initiate renal compensatory mechanisms fail to affect NHE in grey seals. This suggests that control of NHE is not an effector mechanism for regulation of water balance in grey seals.

Administration, Oral↗

Antimasking aspects of harp seal (Pagophilus groenlandicus) underwater vocalizations.

Underwater sounds are very important in social communication of harp seals (Pagophilus groenlandicus) because they are the main means of long- and short-distance communication. Individual harp seals must try to avoid being masked and emit only those calls that will benefit them. Underwater vocalizations of harp seals were recorded during the breeding season. The physical characteristics associated with antimasking attributes of 16 call types were examined. Rising frequency or increasing amplitude within calls were not common. Most of the calls ended abruptly (range 145-966 dB/s), but call onset was more gradual. At high calling rates (95.1-135 calls/min) there were significantly more calls overlapping temporally than at medium (75.1-95 calls/min) or low (35-75 calls/min) calling rates, but even at the highest calling rates, 79.1% of the calls were not overlapped. When 2, 3, or 4 calls overlapped, there were significantly fewer frequency separations of less than 1/3 octave than would be expected by chance. This is important because sounds that are separated by less than 1/3 octave likely mask each other. When 2-4 calls are occurring simultaneously, only 4.5% to 14.2% are masked by virtue of being within 1/3 octave from their nearest neighbor. None of the overlappping calls was of the same type. This suggests that the seals are actively listening to each other's calls and are not randomly using the different call types. Harp seals use frequency and temporal separation in conjunction with a wide vocal repertoire to avoid masking each other.

Animal Communication↗

Tolerance by ringed seals (Phoca hispida) to impact pipe-driving and construction sounds at an oil production island.

During June and July 2000, impact pipe-driving sounds at Northstar Island (Prudhoe Bay, Alaska) were recorded underwater and in air at distances 63-3000 m from the source. Simultaneously, reactions of nearby ringed seals (in water or on ice) were documented. Pipe-driving pulses were analyzed to determine unweighted peak and rms sound-pressure levels (SPLs) and sound-exposure levels (SELs). Underwater, mean levels for these parameters reached 157 and 151 dB re: 1 microPa and 145 dB re: 1 microPa2 x s, respectively, at 63 m. The corresponding values in air were 112 and 96 dB re: 20 microPa and 90 dB re: (20 microPa)2 x s, respectively. Underwater SPLs were <180 dB re: 1 microPa at all distances. During 55 h of observation, 23 observed seals exhibited little or no reaction to any industrial noise except approaching Bell 212 helicopters. Ringed seals swam in open water near the island throughout construction activities and as close as 46 m from the pipe-driving operation. Based on current audiometric data for seals, these sounds are expected to be audible to less than 3 km underwater and at least 0.5 km in air. Most likely the seals around Northstar Island were habituated to industrial sounds.

Acoustics↗

Descending frequency swept tones have lower thresholds than ascending frequency swept tones for a harbor seal (Phoca vitulina) and human listeners.

Many seal vocalizations consist of frequency swept tones. The signal detection thresholds of a harbor seal (Phoca vitulina) and of human listeners were measured using ascending and descending frequency swept tones at 1/3- and 1-oct bandwidths. The swept tones increased or decreased exponentially and traversed the same frequency range. The sweeps were centered on 2, 4, and 8 kHz for the seal study and 0.5, 1, and 2 kHz for the human listeners. The bandwidth of the sweep did not affect signal detection abilities of either the seal or human listeners. The seal had lower signal detection thresholds (1-5 dB) when presented with the descending frequency swept tones (F = 32.04, df = (1,31), p < 0.000001). Human listeners also had lower detection thresholds for descending frequency swept tones (t = -4.78, df = 52, p < 0.0001). Pinniped ascending frequency swept calls may not function as well as descending frequency sweeps for long-distance communicative signals.

Adult↗

Age-related disease in recurrent outbreak of phocid herpesvirus type-1 infections in a seal rehabilitation centre: evaluation of diagnostic methods.

The prevalence and clinical signs of phocid herpesvirus type-1 (PhHV-1) infections among harbour seals (Phoca vitulina) in a seal rehabilitation centre in the Netherlands were monitored between June and September 1993 and 1994 when 34 and 36 seals, respectively, were rehabilitated. In both years PhHV-1-related disease outbreaks occurred in the pupping season. PhHV-1 infections were diagnosed by the demonstration of a more than four-fold increase in virus neutralising serum antibodies in paired serum samples, by the isolation of the virus from swab samples in primary seal kidney cells, and by the detection of PhHV-1 DNA with a polymerase chain reaction (PCR) assay in swab samples. This assay targets a 290 bp fragment of the glycoprotein D (gD) gene equivalent of PhHV-1. The PCR assay when combined with Southern blotting (PCR-SB) was approximately 1000 times more sensitive than virus isolation when tested with serially diluted samples from PhHV-1-infected cell cultures. In contrast with virus isolation, the PCR-SB scored as positive all the animals with serological evidence of PhHV-1 infection. The majority of seals present in the centre during the outbreaks contracted the infection and developed benign upper respiratory disease. However, the severity of PhHV-1-related disease was inversely correlated with age and fatal generalised infections occurred only in neonates.

Age Factors↗

Field immobilisation of southern elephant seals with intravenous tiletamine and zolazepam.

Southern elephant seals (Miroungo leonina) were immobilised with a mixture of tiletamine and zolazepam administered intravenously at a mean (sd) dose rate of 0.46 (0.08) mg/kg. This dose provided a satisfactory degree of anaesthesia with no side effects, and the induction, duration and recovery times were short. The mean (sd) induction time was 26 (9) seconds and the mean level of anaesthesia was 4.4 units on an eight-point scale. Male seals were given less drug than female seals, remained immobilised for shorter periods and recovered sooner. The mean (sd) dose of drug administered to males was 0.44 (0.06) mg/kg and to females 0.48 (0.08) mg/kg, and the mean (sd) duration times were 14.9 (4.5) minutes and 16.1 (5.3) minutes. The mean (sd) time taken to recover from immobilisation was 14.5 (4.6) minutes for males and 15.7 (5.3) minutes for females. Physiological condition and size significantly affected the duration of anaesthesia. Thin seals remained immobilised for 18 (7) minutes whereas fatter seals remained immobilised for 15 (4) minutes (P<0.0001).

Anesthetics, Dissociative↗

Molecular cloning and expression of leptin in gray and harbor seal blubber, bone marrow, and lung and its potential role in marine mammal respiratory physiology.

Leptin is a multifunctional hormone, produced predominantly in adipocytes. It regulates energy balance through its impact on appetite and fat metabolism, and its concentration indicates the size of body fat reserves. Leptin also plays a vital role in stretch-induced surfactant production during alveolar development in the fetus. The structure, expression pattern, and role of leptin have not previously been explored in marine mammals. Phocid seals undergo cyclical changes in body composition as a result of prolonged fasting and intensive foraging bouts and experience rapid, dramatic, and repeated changes in lung volume during diving. Here, we report the tissue-specific expression pattern of leptin in these animals. This is the first demonstration of leptin expression in the lung tissue of a mature mammal, in addition to its expression in the blubber and bone marrow, in common with other animals. We propose a role for leptin in seal pulmonary surfactant production, in addition to its likely role in long-term energy balance. We identify substitutions in the phocine leptin sequence in regions normally highly conserved between widely distinct vertebrate groups, and, using a purified seal leptin antiserum, we confirm the presence of the leptin protein in gray seal lung and serum fractions. Finally, we report the substantial inadequacies of using heterologous antibodies to measure leptin in unextracted gray seal serum.

Adipose Tissue↗

Microcomputer-assisted metabolic studies of voluntary diving of Weddell seals.

Utilizing a microprocessor-controlled peristaltic withdrawal pump, arterial blood samples were obtained from Weddell seals (Leptonychotes weddelli) while diving voluntarily under the sea ice at McMurdo Sound, Antarctica. Plasma concentrations of glucose, lactate, free fatty acids, urea, and amino acids were determined in seals at various times during rest, diving, and recovery. In addition, radiolabeled palmitate, glucose, lactate, p-aminohippurate, inulin, galactose, and cholate were injected into the descending aorta of seals in the resting state or during voluntary diving at sea. Sequential plasma samples were collected, and the kinetics of wash-in and clearance of each component were determined. Under resting conditions, the change in specific activity of palmitate, glucose, and lactate after bolus injection followed smooth multiexponential decay kinetics as in terrestrial animals. Similar decay curves for the clearance of organ-specific compounds were also obtained in seals at rest. If, during voluntary diving, Weddell seals were analogous to exercising animals, the wash-in and clearance kinetics of all metabolites and organ-specific compounds would be qualitatively similar to those observed at rest. In contrast, wash-in and clearance appeared to be qualitatively and quantitatively modified in a way consistent with utilization of the classical Scholander diving response in both short and long dives.

Amino Acids↗

Short-term duodenal seal oil administration normalised n-6 to n-3 fatty acid ratio in rectal mucosa and ameliorated bodily pain in patients with inflammatory bowel disease.

BACKGROUND: A high dietary intake of n-6 compared to n-3 fatty acids (FAs) may promote the production of pro-inflammatory eicosanoids and cytokines. In two recent studies, short-term (10-day) duodenal administration of n-3 polyunsaturated fatty acid rich seal oil ameliorated joint pain in patients with inflammatory bowel disease (IBD). Using unpublished data from these two studies we here investigated whether normalisation of the n-6 to n-3 FA ratio in blood and tissues by seal oil administration was associated with improved health related quality of life (HRQOL) as assessed by the generic short-form 36 (SF-36) questionnaire. RESULTS: In the first pilot study, baseline n-6 to n-3 FA ratio in rectal mucosal biopsies from 10 patients with IBD (9 of those had joint pain) was significantly increased compared with that in 10 control patients without IBD or joint pain. Following seal oil administration, the n-6 to n-3 FA ratio of the IBD-patients was significantly lowered to the level seen in untreated controls. In the subsequent, randomized controlled study (n = 19), seal oil administration reduced the n-6 to n-3 FA ratio in blood similarly and also the SF-36 assessed bodily pain, while n-6 FA rich soy oil administration had no such effect. CONCLUSION: In these two separate studies, short-term duodenal administration of seal oil normalised the n-6 to n-3 FA ratio in rectal mucosa and improved the bodily pain dimension of HRQOL of patients with IBD-related joint pain. The possibility of a causal relationship between n-6 to n-3 FA ratio in rectal mucosa and bodily pain in IBD-patients warrants further investigations.

Aged↗

Attenuation of ciclosporin-induced nephrotoxicity by dietary supplementation of seal oil in Sprague-Dawley rats.

Fish oil, rich in omega-3 (n-3) polyunsaturated fatty acids (PUFAs), has been reported to attenuate nephrotoxicity induced by ciclosporin (cyclosporine A). Harp seal oil is a rich source of n-3 PUFAs. This study investigated the ability of dietary seal oil to reduce nephrotoxicity caused by ciclosporin. Sprague-Dawley rats were maintained on a standard diet (with sunflower oil as lipid, SFO) or a diet enriched with seal oil (with 85% seal oil and 15% sunflower oil as lipid, SO) for four weeks before and four weeks after intravenous administration of ciclosporin (15 mg kg(-1) daily). Kidney function was assessed by measuring blood urea nitrogen, creatinine clearance, urinary N-acetyl-1-beta-D-glucosaminidase, 6-keto-prostaglandin F(1alpha), thromboxane B(2) and malondialdehyde. Systolic blood pressure (SBP) was monitored. Ciclosporin concentrations in blood were measured using liquid chromatographytandem mass spectrometry (LC-MS/MS). The fatty acid compositions of the diets and erythrocyte membranes were analysed by gas chromatography (GC). The results showed that nephrotoxicity was induced by ciclosporin in rats maintained on both SO and SFO diets. However, rats fed on SO diet endured less toxicity than those on SFO diet. The n-3 and n-6 PUFAs in the erythrocyte membrane of rats maintained on SO diet were found to be 10.79% and 11.93%, while those in rats maintained on SFO diet were found to be 1.67% and 22.71%, respectively. In conclusion, dietary supplementation of seal oil was found to reduce ciclosporin-induced nephrotoxicity in rats.

6-Ketoprostaglandin F1 alpha↗

Immunohistochemical fiber typing of harbor seal skeletal muscle.

There is strong evidence that pinnipeds maintain a lipid-based, aerobic metabolism during diving. However, the few fiber-typing studies performed on pinniped skeletal muscles are not consistent with an aerobic physiological profile. The objective of this study was to reexamine the fiber type distribution throughout the primary locomotory muscles of the harbor seal Phoca vitulina. Results from immunohistochemical (IHC) fiber typing indicated that harbor seal swimming muscles (the epaxial muscles) are composed of 47.4% type I (slow twitch, oxidative) fibers and 52.8% IIa (fast twitch, oxidative) fibers, which are homogeneously distributed throughout the muscle. Harbor seal pectoralis, a secondary swimming muscle, was composed of 16.2% type I and 84.3% type IIa fibers. No fast twitch, glycolytic (type IIb) fibers were detected in either muscle, in contrast to published data on fiber typing of harbor seal epaxial muscles using traditional histochemical techniques. The extreme specificity inherent in the IHC fiber typing procedure leads us to conclude that harbor seal swimming muscle is entirely composed of oxidative fibers. Our results are consistent with the enzymatic analyses of pinniped skeletal muscle that support the use of lipid-derived aerobic catabolism to fuel working muscle during diving in these marine mammals.

Analysis of Variance↗

Metabolic rates of captive grey seals during voluntary diving.

The energetic cost of diving in marine mammals is a difficult value to derive given the problems of assessing metabolic rate for an animal at sea. Nevertheless, it is fundamental to our understanding of the foraging strategies of air-breathers exploiting underwater food sources. We measured the metabolic rates of eight captive grey seals, voluntarily diving in a quasi-natural setting. Oxygen consumption during post-dive surface periods was measured using open-flow respirometry, and dive behaviour of the seals was recorded using time depth recorders (TDRs). Mean diving metabolic rate (DMR) for both adults and juveniles was 1.7 times the predicted standard metabolic rate of terrestrial animals of equal size. For all animals, DMR was lower than the rate of metabolism measured whilst they were resting at the water's surface. On a dive-by-dive basis, DMR decreased with dive duration but increased with mean swim speed. Regressing the maximum 5% of DMRs against dive duration resulted in a significant negative relationship that was not significantly different from the relationship between the calculated maximum rate of aerobic metabolism and dive duration, suggesting that these seals were diving within, and up to, their aerobic limits. We developed a model that allows the prediction of DMR from information on dive behaviour of the type routinely collected in telemetry studies of wild seals. The model accurately predicts DMR using behavioural data from periods of diving with known metabolism data. This model can be used to predict the at-sea metabolic rate of wild grey seals, an important input into ecosystem models.

Animals↗

Cardiac responses of grey seals during diving at sea.

Heart rate, swimming speed and diving depth data were collected from free-ranging grey seals, Halichoerus grypus, as they foraged and travelled in the sea around the Hebrides Islands off western Scotland. Information was collected on a tracking yacht using a combination of sonic and radio telemetry. Diving heart rate declined as a function of dive duration. In long dives, grey seals employed extreme bradycardia, with heart rates falling to 4 beats min-1 for extended periods, despite the animal being free to breath at will. This extreme dive response is part of the normal foraging behaviour. Seals spent 89% of the time submerged during bouts of long dives; swimming was restricted to ascent and descent. Dive durations exceeded estimated aerobic dive limit, even assuming resting metabolic rates. These results indicate that behavioural, and possibly cellular, energy-sparing mechanisms play an important role in diving behaviour of grey seals. This has implications not only for studies of mammalian energetics but also for our understanding of the foraging tactics and prey selection of marine mammals. If some seals are using energy-sparing mechanisms to reduce metabolic costs while at depth, they may be forced to wait for and ambush prey rather than to search for and chase it.

Animals↗

Gas exchange of captive freely diving grey seals (Halichoerus grypus).

When at sea, phocids dive for long periods and spend a high percentage of their time submerged. This behaviour requires some combination of an increased oxygen storage capacity, rapid oxygen loading at the surface and reduced oxygen utilisation when submerged. To assess these adaptations, breath-by-breath ventilation was studied in four adult grey seals (two male, two female, 160-250 kg), freely diving in a large outdoor tank where surface access was restricted to one breathing hole. The dive patterns obtained were similar to those recorded from freely diving wild grey seals. Respiratory frequency during the surface periods was 40% higher than that estimated from allometric relationships (19.4 +/- 0.7 breaths min-1), and tidal volume (6.3 +/- 1.21) was approximately five times higher than that estimated from allometric relationships. These adaptations produce a high minute volume and enable gas exchange to occur at the surface. Mean oxygen consumption rate (VO2, measured for a dive+surface cycle) decreased with increasing dive duration. The aerobic dive limit was estimated as 9.6 min for a 150 kg grey seal (using the overall average VO2 of 5.2 ml O2 min-1 kg-1), which is consistent with results from freely diving wild grey seals (only 6% of dives exceeded 10 min). End-tidal oxygen values varied during a surface period, following a U-shaped curve, which suggests that there is limited oxygen uptake from the lung and/or blood oxygen stores during dives. This result was unexpected and indicates that these seals are utilising substantial physiological responses to conserve oxygen, even during shallow voluntary diving.

Animals↗

Ambient temperature does not affect the tactile sensitivity of mystacial vibrissae in harbour seals.

Vibrissae provide pinnipeds with tactile information primarily in the aquatic environment, which is characterized by its high thermal conductivity and large potential cooling power. Since studies of thermal effects on human tactile sensitivity have revealed that cooling below normal skin temperature impairs sensitivity, the present study investigates the tactile sensitivity of the vibrissal system of harbour seals at varying ambient temperatures. Using plates bearing gratings of alternating grooves and ridges, the texture difference thresholds of two adult seals were determined under water. We took advantage of the natural difference in ambient temperature between summer and winter. Mean water temperature was 1. 2 degreesC during the winter and 22 degreesC during the summer. During the cold season, the thermal status of both seals was examined using an infrared-sensitive camera system. The texture difference threshold of both seals remained the same (0.18 mm groove width difference) under both test conditions. The thermographic examination revealed that the skin areas of the head where the mystacial and supraorbital vibrissae are located show a substantially higher degree of thermal emission than do adjacent skin areas. This suggests that, in the vibrissal follicles of harbour seals, no vasoconstriction occurs during cold acclimation, so that the appropriate operating temperature for the mechanoreceptors is maintained.

Acclimatization↗

Lymphatic absorption of seal and fish oils and their effect on lipid metabolism and eicosanoid production in rats.

Eicosapentaenoic (EPA) and docosahexaenoic acids (DHA) were distributed mainly in the sn-1 and 3 positions of seal oil triglyceride and in the sn-2 position of fish oil triglyceride. In Expt. 1, the structural distribution of EPA and DHA in lymph triglyceride of rats given seal or fish oils was similar to the distribution in the administered oils. In Expt. 2, seal oil-rich or fish oil-rich fats having constant polyunsaturated/monounsaturated/saturated fatty acids and n-6/n-3 polyunsaturated fatty acids ratios were fed to rats for 3 weeks. Seal oil more effectively reduced plasma and liver triglyceride than fish oil. Ratio of the productions of aortic prostacyclin and platelet thromboxane A2 stimulated by thrombin was significantly higher in rats fed seal oil than in those fed fish oil. The results suggested that the different intramolecular distribution of EPA and DHA in dietary fat affected lipid metabolism differently in rats.

Absorption↗

Changes in plasma progesterone and prolactin concentrations during the annual cycle and the role of prolactin in the maintenance of lactation and luteal development in the Antarctic fur seal (Arctocephalus gazella).

Progesterone in Antarctic fur seals was undetectable from 1-2 days before parturition to 4-6 days after parturition. There was a rapid increase in progesterone to 20 ng/ml between 6 and 10 days post partum and this increase coincided with peak concentrations of oestradiol-17 beta at the time normally associated with oestrus and mating in this species. Newly formed corpora lutea were present in the ovaries by Day 9 post partum even though the seals had been isolated in an enclosure and not mated. Thereafter, progesterone remained detectable, but at a low concentration (5 ng/ml) throughout embryonic diapause. A similar pattern was observed in unmated females which suggests they enter a period of pseudopregnancy. Progesterone increased to 35 ng/ml between late February and mid-March, indicating activation of the corpus luteum at the end of diapause, and then declined slowly through the remainder of gestation. Plasma prolactin, measured against a human prolactin standard, was elevated from 1-2 days before parturition and peaked at 0-3 days post partum. It then declined slowly throughout the post-partum period and remained at a low level throughout embryonic diapause. Prolactin concentration declined to undetectable at the end of diapause and before the end of lactation. Reduction of prolactin secretion by injections of bromocriptine from Days 3 to 5 post-partum terminated lactation. Mothers, which normally leave their pups to feed at sea on about Day 7 post partum, did not continue to lactate beyond Day 7 although this did not appear to be associated with reduced prolactin secretion. Bromocriptine treatment appeared to prevent the post-ovulatory surge of progesterone although there was no long-term effect of bromocriptine on progesterone secretion during the early stages of embryonic diapause/pseudopregnancy. This study has shown that prolactin is an important hormone for maintaining early lactation in the fur seal and it probably also has a role in the control of ovulation and luteal development. Prolactin does not appear to be implicated in the control of lactation cycles in fur seals. Changes in plasma progesterone during the annual cycle show that the pattern in fur seals resembles that of some carnivores with embryonic diapause.

Animals↗