Simon D. Goldsworthy

Postsealing genetic variation and population structure of two species of fur seal (Arctocephalus gazella and A. tropicalis)

Commercial sealing in the 18th and 19th centuries had a major impact on the Antarctic and subantarctic fur seal populations (Arctocephalus gazella and A. tropicalis) in the Southern Ocean. The intensive and unrestricted nature of the industry ensured substantial reductions in population sizes and resulted in both species becoming locally extinct at some sites. However, both species are continuing to recover, through the recolonization of islands across their former range and increasing population size. This study investigated the extent and pattern of genetic variation in each species to examine the hypothesis that higher levels of historic sealing in A. gazella have resulted in a greater loss of genetic variability and population structure compared with A. tropicalis. A 316‐bp section of the mitochondrial control region was sequenced and revealed nucleotide diversities of 3.2% and 4.8% for A. gazella and A. tropicalis, respectively. There was no geographical distribution of lineages observed within either species, although the respective ΦST values of 0.074 and 0.19 were significantly greater than zero. These data indicate low levels of population structure in A. gazella and relatively high levels in A. tropicalis. Additional samples screened with restriction endonucleases were incorporated, and the distribution of restriction fragment length polymorphism (RFLP) and sequence haplotypes were examined to identify the main source populations of newly recolonized islands. For A. tropicalis, the data suggest that Macquarie Island and Iles Crozet were probably recolonized by females from Marion Island, and to a lesser extent Ile Amsterdam. Although there was less population structure within A. gazella, there were two geographical regions identified: a western region containing the populations of South Georgia and Bouvetøya, which were the probable sources for populations at Marion, the South Shetland and Heard Islands; and an eastern region containing the panmictic populations of Iles Kerguelen and Macquarie Island. The latter region may be a result of a pronounced founder effect, or represent a remnant population that survived sealing at Iles Kerguelen.

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 F1, 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.

Sex differences in mass loss rate and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups at Macquarie Island

Abstract We investigated the relationship between the mass gained by a pup during a period of maternal attendance (as an index of milk intake) and the duration of the preceding foraging trip in relation to the mass-specific rate of mass loss during fasting periods and the growth rate of Antarctic fur seal (Arctocephalus gazella) pups at Macquarie Island. We found that (1) serially weighed male pups grew significantly faster than females pups and that (2) fasting female pups lost mass at a significantly higher rate (2.55% day−1) than male pups (2.12% day−1) of the same mass; (3) during periods of maternal attendance, there were no intersexual differences in the amount of mass gained by pups of the same size, hence (4) female pups required a higher daily mass gain to grow at the same rate as male pups. Our results show that intersexual differences in growth rate may be accounted for by intersexual differences in mass-specific rate of mass loss, because females lost 0.42% more of their total mass per day (i.e. 4.2 g kg−1 day−1) compared with male pups of the same body mass. Despite intersexual differences in growth rates, our results indicate equality of maternal expenditure between the sexes. Intersexual differences in the rate of mass loss may be due to differences in the metabolic rate, activity level and/or body composition of male and female pups.

Energy content of mesopelagic fish from Macquarie Island.

The water and calorific content of fifteen species of mesopelagic sub-Antarctic fish from Macquarie Island were determined. Mean percent water content was 69–82%. Calorific content was highly variable between species, especially in the Myctophidae, where it ranged between 22.6–59.3 kJ·g−1 dry weight. The water and calorific content varied with size class within a species, with the smallest size classes generally having the lowest water content but highest calorific content. These values will be useful for future assessment of energetic transfer between trophic levels and energetic modelling of Southern Ocean ecosystems.

Lower reproductive success in hybrid fur seal males indicates fitness costs to hybridization

Hybridization among organisms can potentially contribute to the processes of evolution, but this depends on the fitness of hybrids relative to parental species. A small, recently formed population of fur seals on subantarctic Macquarie Island contains a high proportion of hybrids (17–30%) derived from combinations of three parental species: Antarctic, subantarctic and New Zealand fur seals. Mitochondrial control‐region data (restriction fragment length polymorphisms) and nine microsatellites were used to determine the species composition of breeding adults, and hybrid male fitness was measured by comparing reproductive success (number of genetically inferred paternities) of hybrid and pure‐species territory males over 6 years. No correlations were found between male reproductive success and three genetic measures of outbreeding, but this may be due to a relatively small number of dominant males analysed. Territory males fathered 63% of pups, but hybrid males had lower reproductive success than pure‐species males despite having the same ability to hold territories. A greater proportion of females in hybrid male territories conceived extra‐territorially than those in territories of pure‐species males, and most (70 of 82) mated with conspecifics. This suggests the presence of reproductive isolating mechanisms that promote positive assortative mating and reduce the production of hybrid offspring. Although we found no evidence for male sterility in the population, mechanisms that reduce lifetime reproductive success may act to decrease the frequency of hybrids. Our study has identified a disadvantage of hybridization — reduced reproductive success of hybrid sons — that may be contributing to the persistence of pure lineages at Macquarie Island and the temporal decline in hybridization observed there.

Diet of Patagonian toothfish (Dissostichus eleginoides) around Macquarie Island, South Pacific Ocean

A total of 1423 stomach samples were taken from Patagonian toothfish, Dissostichus eleginoides, caught by bottom trawls at two fishing grounds near Macquarie I., over three fishing seasons. Fish were caught at depths ranging from 500 to 1290 m, and ranged in size from 310 to 1490 mm total length. The 462 stomach samples (32%) that contained prey items indicated that toothfish preyed on a broad range of species including fish, cephalopods and crustaceans (58%, 32% and 10% biomass, respectively), suggesting that they are opportunistic predators. The bathypelagic fish Bathylagus sp. was the most important fish prey (14% dietary biomass); however, nototheniid, macrourid, morid and myctophid fish were also taken. The squid Gonatus antarcticus was also an important prey species (16% biomass), and many other cephalopod species were taken in low frequency. Prawnlike crustaceans (Nematocarcinidae, Mysididae, Sergestidae and Euphausiidae) were the most important crustaceans taken (9% of prey biomass). Significant inter-seasonal and inter-fishing-ground differences in diet were found, but dietary composition was not related to fishing depth, fish size (with the exception of one fishing ground in one season) or the time of day of capture. Comparison with other studies reveals biogeographical differences in the diet of toothfish.

Interspecific differences in male vocalizations of three sympatric fur seals (Arctocephalus spp.)

This study investigated species recognition based on bark calls and full threat calls (FTCs) in three fur seal species, Antarctic Arctocephalus gazella, subantarctic A. tropicalis and New Zealand A. forsteri, that breed sympatrically and hybridize at subantarctic Macquarie Island. Bark calls, which are produced by males in male‐female interactions, were more species-specific than their full threat calls, suggesting that bark calls could be used in species recognition and female mate choice. Further, the bark calls of A. tropicalis were more species-specific than those of A. gazella and A. forsteri, suggesting that divergence of calls between species is a consequence of phylogenetic distance, or has resulted from sexual selection through female mate choice. We believe the latter is more probable as we did not observe similar divergence in the FTCs of males. As such, the highly divergent bark calls of A. tropicalis may have resulted from sexual selection that has promoted pre-mating isolation via the process of reinforcement.

INDIVIDUAL VOCAL TRAITS OF MOTHER AND PUP FUR SEALS

ABSTRACT This study investigates individual vocal traits in three species of fur seal: Antarctic fur seal Arctocephalus gazella, Subantarctic fur seal A. tropicalis, New Zealand fur seal A. forsteri and their hybrids. The attraction calls of mothers and pups were highly stereotyped within each individual and markedly different between individuals. Pup attraction calls (emitted by females) were more variable between individual A. tropicalis and A. forsteri than between individual hybrids and A. gazella. However, such a pattern was not evident for female attraction calls (emitted by pups). Pup attraction calls and female attraction calls were both generally tonal calls overlain with regions of pulses. Female attraction calls had relatively high fundamental frequencies. The importance of individual vocalisations for mothers and pups is best appreciated in relation to maternal fitness and offspring survival: individual vocalisations are favoured by natural selection as they facilitate rapid reunion when mothers return from foraging trips, ensuring maternal resources are not invested in unrelated pups.

Drinking behaviour and water turnover rates of Antarctic fur seal pups: implications for the estimation of milk intake by isotopic dilution

The estimation of milk consumption in free-ranging seals using tritium dilution techniques makes the key assumption that the animals drink no pre-formed water during the experimental period. However, frequent observations of unweaned Antarctic fur seal pups drinking water at Iles Kerguelen necessitated the testing of this assumption. We estimated water flux rates of 30 pups (10.7+/-0.3 kg) in four experimental groups by isotopic dilution over 4 days. The groups were: (1) pups held in an open air enclosure without access to water to estimate fasting metabolic water production (MWP); (2) free-ranging pups not administered additional water; (3) pups held in an open air enclosure and given a total of 300 ml of fresh water to verify technique accuracy; and (4) free-ranging pups given 200 ml of fresh water. Pups without access to water exhibited water flux rates (20.5+/-0.8 ml kg(-1)d(-1)), which were significantly lower than those observed for the free-ranging group (33.0+/-1.7 ml kg(-1) d(-1)). Mean estimated pre-formed water intake for the free-ranging experimental groups was 12.6 ml kg(-1) d(-1). Thus, MWP, measured as total water intake during fasting, may be significantly over-estimated in free-ranging Antarctic fur seal pups at Iles Kerguelen and at other sites and subsequently milk intake rates may be underestimated.

Multiple mating strategies explain unexpected genetic mixing of New Zealand fur seals with two congenerics in a recently recolonized population

Human impacts on natural systems can cause local population extinctions, which may promote redistribution of taxa and secondary contact between divergent lineages. In mammalian populations that have mating systems shaped by polygyny and sexual selection, the potential for hybridization to ensue and persist depends on individual and demographic factors. At Macquarie Island, a recently formed fur seal population is comprised of both sexes of breeding Antarctic (Arctocephalus gazella) and subantarctic (A. tropicalis) fur seals, and an itinerant collection of male New Zealand fur seals (A. forsteri), presumed to be non‐breeders due to their absence from principle breeding areas. The mating system of the three species is described as resource‐defence polygyny: males defend beach territories containing breeding females for exclusive mating rights. A recent genetic study identified a high level of hybridization in the population (17–30%), unexpectedly involving all three species. This study examined the source of involvement in breeding by A. forsteri with respect to mating strategies operating in the population. Ninety‐five (10%) pups born from 1992 to 2003 were genetically identified as New Zealand hybrids. Most resulted from reproduction within territories by New Zealand hybrids of both sexes, although some were conceived extra‐territorially, indicating that males successfully utilize strategies other than territory holding to achieve paternities. Female reproductive status influenced mating partner and mating location, and females without pups were more likely to conceive extra‐territorially and with A. forsteri males. This study illustrates an important consequence of low heterospecific discrimination in a sympatric population of long‐lived mammals.