The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups

The physiological and behavioural development of diving was examined in Australian fur seal (Arctocephalus pusillus doriferus) pups to assess whether animals at weaning are capable of exploiting the same resources as adult females. Haematocrit, haemoglobin and myoglobin contents all increased throughout pup development though total body oxygen stores reached only 71% of adult female levels just prior to weaning. Oxygen storage components, however, did not develop at the same pace. Whereas blood oxygen stores had reached adult female levels by 9 months of age, muscle oxygen stores were slower to develop, reaching only 23% of adult levels by this age. Increases in diving behaviour corresponded to the physiological changes observed. Pups spent little time (<8%) in the water prior to moulting (age 1–2 months) whereas following the moult, they spent >27% of time in the water and made mid-water dives (maximum depth 35.7 ± 2.9 m) with durations of 0.35 ± 0.03 min. By 9 months (just prior to weaning), 30.5 ± 9.3% of all dives performed were U-shaped benthic dives (maximum depth 65.0 ± 6.0 m) with mean durations of 0.87 ± 0.25 min, significantly shorter than those of adult females. These results suggest that while Australian fur seal pups approaching the age of weaning are able to reach similar depths as adult females, they do not have the physiological capacity to remain at these depths for sufficient durations to exploit them to the same efficiency.

Pup production and population trends of the Australian fur seal (Arctocephalus pusillus doriferus)

We estimated the number of live Australian fur seal pups using capture-markresights, direct ground counts, or aerial photography at all breeding sites following the pupping season of November-December 2002. Pups were recorded at 17 locations; nine previously known colony sites, one newly recognized colony and seven haul-out sites where pups are occasionally born. In order of size, the colonies were Lady Julia Percy Island (5,899 pups), Seal Rocks (4,882), The Skerries (2,486), Judgment Rocks (2,427), Kanowna Island (2,301), Moriarty Rocks (1,007), Reid Rocks (384), West Moncoeur Island (257), and Tenth Island (124). The newly recognized site was Rag Island, in the Cliffy Group, where we recorded 30 pups. We also recorded pups at the following haul-out sites: Cape Bridge-water (7 pups), Bull Rock (7), Wright Rock (5), Twin Islet (1), The Friars (1), He des Phoques (1), and Montague Island (1). In total, we estimate there were 19,819 (SE = 163) live pups at the time of the counts. We discuss trends in pup numbers and derive current population estimates for the Australian fur seal.

Milk consumption, body composition and pre-weaning growth rates of Australian fur seal

Pre-weaning growth rates, body composition, milk consumption and mass gain efficiency were measured in Australian fur seal Arctocephalus pusillus doriferus pups born in two consecutive breeding periods. Australian fur seals have the highest birth mass of any fur seal species (male 8.3 kg; female 7.2 kg). While their absolute pre-weaning growth rate (male 62 g·day⁻¹; female 53 g·day⁻¹) is similar to that of other temperate latitude fur seals, they have the longest birth-mass doubling time of any otariid species (134–136 days). Daily milk consumption increased from 400 g·day−1 (5 MJ·day−1) after birth to 675 g·day⁻¹ (13.7 MJ·day⁻¹) at age 210 day. However, mean mass-specific milk consumption (41 g·kg⁻¹) is substantially lower than in other otariid species (58–70 g·kg⁻¹) and, combined with a low mass gain efficiency (0.12 g·g⁻¹), contributes to the low mass-specific growth rates observed. There were no significant differences in either absolute or mass-specific milk consumption between the sexes. Significant differences, however, were found between the sexes in the body composition of pups with females generally having larger body lipid stores than males for any given mass. Peak milk yield by Australian fur seal females is estimated at 0.60 MJkg−0.75, substantially less than in Antarctic fur seals. The low level of maternal energy transfer in Australian fur seals may reflect the relatively low marine productivity of their foraging areas.

Chemical characterisation of the oligosaccharides in hooded seal (Cystophora cristata) and Australian fur seal (Arctocephalus pusillus doriferus) milk

Carbohydrates were extracted from hooded seal milk, Crystophora cristata (family Phocidae). Free oligosaccharides were separated by gel filtration and then purified by ion exchange chromatography, gel filtration and preparative thin layer or paper chromatography and their structures determined by ¹H-NMR. The hooded seal milk was found to contain inositol and at least nine oligosaccharides, most of which had lacto-N-neotetraose or lacto-N-neohexaose as core units, similar to those in milk of other species of Carnivora such as bears (Ursidae). Their structures were as follows: Gal(β1-4)Glc (lactose); Fuc(α1-2)Gal(β1-4)Glc (2′-fucosyllactose); Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)Glc (lacto-N-neotetraose); Fuc(α1-2)Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)Glc (lacto-N-fucopentaose IV); Gal(β1-4)GlcNAc(β1-3)[Gal(β1-4)GlcNAc(β1-6)]Gal(1-4)Glc (lacto-N-neohexaose); Fuc(α1-2)Gal(β1-4)GlcNAc(β1-3)[Gal(β1-4)GlcNAc(β1-6)]Gal(β1-4)Glc (monofucosyl lacto-N-neohexaose a); Gal(β1-4)GlcNAc(β1-3)[Fuc(α1-2)Gal(β1-4)GlcNAc(β1-6)]Gal(β1-4)Glc (monofucosyl lacto-N-neohexaose b); Fuc(α1-2)Gal(β1-4)GlcNAc(β1-3)[Fuc(α1-2)Gal(β1-4)GlcNAc(β1-6)]Gal(β1-4)Glc (difucosyl lacto-N-neohexaose); Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)Glc (para lacto-N-neohexaose); Fuc(α1-2)Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)Glc (monofucosyl para lacto-N-neohexaose). Milk of the Australian fur seal, Arctophalus pusillus doriferus (family Otariidae) contained inositol but no lactose or free oligosaccharides. These results, therefore, support the hypothesis that the milk of otariids, unlike that of phocids, contains no free reducing saccharides.

Australian fur seal

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Characterization of Australian fur seal vocalizations during the breeding season

The vocal repertoire, structure, and behavioral context of airborne vocalizations produced by Australian fur seals (Arctocephalus pusillus doriferus) are described using recordings made at a breeding colony on Kanowna Island, Bass Strait, Australia. The study identified six different call types: three produced by males (bark, guttural threat, and submissive call); five produced by females (bark, guttural threat, submissive call, growl, and pup attraction call) and the female attraction call produced by pups and yearlings. Vocalizations were compared according to age and sex classes. The overall structure and function of the pup attraction and female attraction call produced by females, yearlings, and pups, was similar. However, while similar in their overall appearance, certain call types have a lower fundamental frequency when compared with other fur seals. In addition, the male bark call alters in rate of production according to the context used, where calls are slower when males are stationary and advertising their territorial status and faster when males are involved in confrontations with other males or actively herding females. Further research is required to investigate changes in environmental conditions and their effects on shaping the call structure and communication in Australian fur seals.

Terrestrial apnoeas and the development of cardiac control in Australian fur seal (Arctocephalus pusillus doriferus) pups

The development of cardiac control in association with terrestrial respiration patterns was examined throughout the period of maternal dependence in Australian fur seal pups. Resting eupnoic heart rate and respiration rate were significantly correlated (r² = 0.49) and both decreased with age (P < 0.05 in both cases). From an early age (1 month), pups displayed terrestrial apnoeas (18.1 ± 0.5 s) accompanied by substantial bradycardia (127 beats min^-1, a 13% decrease from eupnoic HR). Terrestrial apnoea duration increased significantly with age reaching a mean of 41 s just prior to weaning, slightly lower than the mean dive duration (52 s) previously recorded for pups of the same age. Correspondingly, mean apnoic heart rate decreased with age to 74 beats min^-1 just prior to weaning, representing a 25% decrease on eupnoic heart rate. Importantly, concomitant with the decrease in mean apnoic heart rate with age, an increase in the control
of bradycardia was evident with the variability in instantaneous apnoic heart decreasing such that older pups were able to maintain a low steady heart rate for the duration of the apnoea. The changes seen in these parameters are similar to those reported during postnatal development in elephant seals (Mirounga spp.) and harbour seals (Phoca vitulina), and are considered indicative of the development of cardiac control. These findings suggest a common strategy for the development of bradycardia control in both otariid and phocid seals.

Genetic status of an endemic marine mammal, the Australian fur seal, following historical harvesting

Genetic variation, and the way in which it is partitioned among populations, has implications for a species’ survival and evolutionary potential. Such information is particularly important for the successful conservation and management of species that have experienced past human impacts and potential losses of genetic diversity. Overharvesting of the Australian fur seal Arctocephalus pusillus doriferus in the 18th and 19th centuries resulted in severe population reductions and elimination of an estimated 17 of 26 colonies. Currently, the subspecies is recovering and c. 20 000 pups are produced annually at 13 colony sites, most of which are situated in Bass Strait in south-eastern Australia. Genetic analysis of samples collected from pups captured at nine colonies revealed no difference in allelic diversity or heterozygosity at five microsatellite loci and no differences in haplotype diversity within a 344 bp region of the mitochondrial DNA control region. There was some evidence for isolation by distance but the program STRUCTURE predicted a single cluster of individuals. Gene flow among colonies appears to be substantial at present, indicating that the Australian fur seal is currently a single, panmictic unit.

Changes in muscle composition during the development of diving ability in the Australian fur seal

During development the Australian fur seal transitions from a terrestrial, maternally dependent pup to an adult marine predator. Adult seals have adaptations that allow them to voluntarily dive at depth for long periods, including increased bradycardic control, increased myoglobin levels and haematocrit. To establish whether the profile of skeletal muscle also changes in line with the development of diving ability, biopsy samples were collected from the trapezius muscle of pups, juveniles and adults. The proportions of different fibre types and their oxidative capacity were determined. Only oxidative fibre types (Type I and IIa) were identified, with a significant change in proportions from pup to adult. There was no change in oxidative capacity of Type I and IIa fibres between pups and juveniles but there was a two-fold increase between juveniles and adults. Myoglobin expression increased between pups and juveniles, suggesting improved oxygen delivery, but with no increase in oxidative capacity, oxygen utilisation within the muscle may still be limited. Adult muscle had the highest oxidative capacity, suggesting that fibres are able to effectively utilise available oxygen during prolonged dives. Elevated levels of total creatine in the muscles of juveniles may act as an energy buffer when fibres are transitioning from a fast to slow fibre type.

Morphometric and molecular characterization of the species of Uncinaria Frölich, 1789 (Nematoda) parasitic in the Australian fur seal Arctocephalus pusillus doriferus (Schreber), with notes on hookworms in three other pinniped hosts

This study presents morphological and molecular data on hookworms from the Australian fur seal Arctocephalus pusillus doriferus (Schreber) currently identified in Australian waters as Uncinaria hamiltoni Baylis, 1933. Additional specimens from the Australian sea lion Neophoca cinerea (Péron) and the New Zealand fur seal Arctocephalus forsteri (Lesson) from Australia, and the Southern elephant seal Mirounga leonina (Linnaeus) from Antarctica, were included. Using the internal transcribed spacer (ITS), hookworms from A. p. doriferus, N. cinerea and A. forsteri were found to be genetically similar but distinct from Uncinaria spp. found in M. leonina from Antarctica, as well as from Zalophus californianus (Lesson) and Callorhinus ursinus (Linnaeus) from California. Few morphological differences were detected between these taxa.

Age-related differences revealed in Australian fur seal Arctocephalus pusillus doriferus gut microbiota

The gut microbiota of Australian fur seals (Arctocephalus pusillus doriferus) was examined at different age classes using fluorescent in situ hybridisation (FISH) and 16S rRNA gene pyrosequencing. The FISH results indicated that in the fur seal groups, the predominant phyla are Firmicutes (22.14-67.33%) followed by Bacteroidetes (3.11-15.45%) and then Actinobacteria (1.4-5.9%) consistent with other mammals. Phylum Proteobacteria had an initial abundance of 1.8% in the 2-month-old pups, but < 1% of bacterial numbers for the other fur seal age groups. Significant differences did occur in the abundance of Clostridia, Lactobacilli and Bifidobacteria between 2 months pups and 9 months pups and adult fur seals. Results from the 16S rRNA gene pyrosequencing supported the FISH data and identified significant differences in the composition of Firmicutes, Bacteroidetes, Actinobacteria, Proteobacteria, Verrucomicrobia and Fusobacteria at all ages. Class Clostridia in phylum Firmicutes dominates the microbiota of the 2 months and 9 months seal pups, whilst class Bacilli dominates the 6 months pups. In addition, a high level of dissimilarity was observed between all age classes. This study provides novel insight into the gut microbiota of Australian fur seals at different age classes.

Effect of proximity to the shelf edge on the diet of female Australian fur seals

The Australian fur seal Arctocephalus pusillus doriferus is a temperate latitude species with a breeding distribution restricted to Bass Strait, Australia. Recent studies of the foraging behaviour of female Australian fur seals indicated that they feed demersally in the shallow continental shelf waters, a behaviour that is in contrast to the epipelagic foraging of females of most other arctocephaline (Southern Hemisphere fur seals) species and akin to that observed in sea lions. These studies, however, were conducted at one colony (Kanowna Island) located in central northern Bass Strait, and it was suggested that the observed foraging behaviour may have been due to the distance of this colony from the continental shelf edge (180 km), making it inefficient to forage beyond it. Here, the diet of lactating Australian fur seals was compared between 2 colonies to test if differing proximity to the continental shelf edge resulted in differences in foraging behaviour. The 2 breeding colonies studied, Kanowna Island and The Skerries, were 180 and 25 km from the nearest shelf edge, respectively. We analysed a total of 917 scat samples collected at the 2 colonies between 1997 and 2001. From faecal analysis, 45 primarily demersal on-shelf species of fishes and cephalopods were identified. Only 4 species had a frequency of occurrence greater than 10%: redbait Emmelichthys nitidus, jack mackerel Trachurus sp., red rock cod Pseudophycis bachus, and Gould’s squid Nototodarus gouldi. No seasonal, annual or spatial differences were found between the 2 colonies, indicating that proximity to the shelf edge does not influence diet.