Australian Sea Lion Pups Research Articles

Mitigating disease risk in an endangered pinniped: early hookworm elimination optimizes the growth and health of Australian sea lion pups.

The Australian sea lion (Neophoca cinerea) experiences high pup mortality of seasonally alternating severity, partly attributed to endemic hookworm (Uncinaria sanguinis) infection. To further explore health outcomes of early hookworm elimination, a treatment trial was conducted at Seal Bay Conservation Park, South Australia, over consecutive lower and higher mortality breeding seasons (2019, 19.2%; 2020-1; 28.9%). Pups (n = 322) were stratified into two age cohorts (median 14 d and 24 d recruitment ages) and randomly assigned to treated (topical ivermectin 500 μg/kg) or control (untreated) groups. A younger prepatent cohort <14 d old (median 10 d) was identified a posteriori. A seasonally independent growth benefit resulted from hookworm elimination across all age cohorts. The greatest relative improvements (bodyweight + 34.2%, standard length + 42.1%; p ≤ 0.001) occurred in the month post-treatment, in the youngest prepatent cohort. A significant benefit of lesser magnitude (bodyweight + 8.6-11.6%, standard length + 9.5-18.4%; p ≤ 0.033) persisted up to 3 months across all age cohorts - greatest in the youngest pups. Treatment resulted in immediate improvement in hematological measures of health - decreased anemia and inflammation severity (p ≤ 0.012). These results enhance our understanding of host-parasite-environment interactions within the context of hematological ontogenesis, confirm the seasonally independent benefits of hookworm disease intervention, and further inform conservation recommendations for this endangered species.

Gut microbiota of endangered Australian sea lion pups is unchanged by topical ivermectin treatment for endemic hookworm infection.

The gut microbiota is essential for the development and maintenance of the hosts' immune system. Disturbances to the gut microbiota in early life stages can result in long-lasting impacts on host health. This study aimed to determine if topical ivermectin treatment for endemic hookworm (Uncinaria sanguinis) infection in endangered Australian sea lion (Neophoca cinerea) pups resulted in gut microbial changes. The gut microbiota was characterised for untreated (control) (n = 23) and treated (n = 23) Australian sea lion pups sampled during the 2019 and 2020/21 breeding seasons at Seal Bay, Kangaroo Island. Samples were collected pre- and post-treatment on up to four occasions over a four-to-five-month period. The gut microbiota of untreated (control) and treated pups in both seasons was dominated by five bacterial phyla, Fusobacteria, Firmicutes, Proteobacteria, Actinobacteria and Bacteroidetes. A significant difference in alpha diversity between treatment groups was seen in pups sampled during the 2020/21 breeding season (p = 0.008), with higher richness and diversity in treated pups. Modelling the impact of individual pup identification (ID), capture, pup weight (kg), standard length (cm), age and sex on beta diversity revealed that pup ID accounted for most of the variation (35% in 2019 and 42% in 2020/21), with pup ID, capture, and age being the only significant contributors to microbial variation (p < 0.05). There were no statistically significant differences in the composition of the microbiota between treatment groups in both the 2019 and 2020/21 breeding seasons, indicating that topical ivermectin treatment did not alter the composition of the gut microbiota. To our knowledge, this is the first study to characterise the gut microbiota of free-ranging Australian pinniped pups, compare the composition across multiple time points, and to consider the impact of parasitic treatment on overall diversity and microbial composition of the gut microbiota. Importantly, the lack of compositional changes in the gut microbiota with treatment support the utility of topical ivermectin as a safe and minimally invasive management strategy to enhance pup survival in this endangered species.

Developing Immune Profiles of Endangered Australian Sea Lion (Neophoca cinerea) Pups Within the Context of Endemic Hookworm (Uncinaria sanguinis) Infection.

As a top predator, the endangered Australian sea lion (Neophoca cinerea) is a sentinel of ecosystem change, where population trends can reflect broader shifts in the marine environment. The population of this endemic pinniped was historically diminished by commercial sealing, and recovery has been slowed by fishery interactions, disease and, potentially, pollutants. Hookworm infects 100% of neonatal pups and has been identified as a contributor to population decline. Here, a multivariable approach using traditional serological and novel molecular tools such as qPCR and ddPCR was used to examine immune phenotypes of developing Australian sea lion pups infected with the endemic hookworm (Uncinaria sanguinis) from two South Australian colonies. Results show changing immunophenotypes throughout the patent period of infection represented by pro-inflammatory cytokines (IL-6), IgG and acute-phase proteins. Although cytokines may prove useful as markers of resistance, in this study, IL-6 is determined to be an early biomarker of inflammation in Australian sea lion pups, excluding the alternative hypothesis. Additionally, immunological differences between animals from high- and low-intensity hookworm seasons, as well as ivermectin-treated animals, indicate hookworm infection modulation of the host immune response, as evidenced by a lower IL-6 mRNA expression in the non-treated groups. This study of the Australian sea lion is an example of an ecoimmunological approach to disease investigation, which can be applied to evaluate the impact of environmental and anthropogenic factors on susceptibility to infectious diseases in free-ranging species

Chemical Profiles of Integumentary and Glandular Substrates in Australian Sea Lion Pups (Neophoca cinerea).

Recognition of individuals or classes of individuals plays an important role in the communication systems of many mammals. The ability of otariid (i.e., fur seal and sea lion) females to locate and identify their offspring in colonies after returning from regular foraging trips is essential to successful pup rearing. It has been shown that olfaction is used to confirm the identity of the pup by the mother when they reunite, yet the processes by which this chemical recognition occurs remain unclear. Using gas chromatography-mass spectrometry, we examined chemical profiles of integumentary and glandular secretions/excretions from pre- and post-molt Australian sea lion pups (Neophoca cinerea) and compared fur and swab samples to assess data collection methods. Multivariate statistics were applied to assess differences in chemical composition between body regions and sexes. We found differences among secretions from various body regions, driven by the distinctiveness of the oral odor mixture. The fine-scale trends in pre- and post-molt pups seem to differ due to changes in the behavior of pups and consequent decrease in the transfer of compounds among adjacent body regions in older pups. Volatile compounds from exocrine substrates were not distinct for different sexes. We also show that swab samples provide better data for exploring social olfaction than fur samples for this species. Obtaining fundamental chemical information, in this case chemical profiles of animals, and discerning differences in chemical composition is an important step toward fully exploring the intricacies of mother-offspring olfactory recognition and its underlying processes.

Visual cues do not enhance sea lion pups\u2019 response to multimodal maternal cues

Mammals use multiple sensory cues for mother-offspring recognition. While the role of single sensory cues has been well studied, we lack information about how multiple cues produced by mothers are integrated by their offspring. Knowing that Australian sea lion (Neophoca cinerea) pups recognise their mother’s calls, we first tested whether visual cues are used by pups to discriminate between conspecifics of different age classes (adult female vs pup). We then examined if adding a visual stimulus to an acoustic cue enhances vocal responsiveness of Australian sea lion pups, by presenting wild individuals with either a visual cue (female 3D-model), an acoustic cue (mother’s call), or both simultaneously, and observing their reaction. We showed that visual cues can be used by pups to distinguish adult females from other individuals, however we found no enhancement effect of these cues on the response in a multimodal scenario. Audio-only cues prompted a similar reaction to audio-visual cues that was significantly stronger than pup response to visual-only cues. Our results suggest that visual cues are dominated by acoustic cues and that pups rely on the latter in mother recognition.

When were the weaners weaned? Identifying the onset of Australian sea lion nutritional independence

Weaning in mammals is typically thought of as the transition from reliance on maternal milk to feeding independently. Current theory suggests a complex process involving mothers imparting enough resources to offspring as to ensure survival without compromising both prior and future reproductive efforts, and the demands of offspring whose primary concern is survival. Otariid seals are a suitable group to study this given the morphological and behavioral similarities across species of the primary care giver, adult females. At higher latitudes, the duration of maternal care is short and tightly linked to seasonal productivity of the marine environment, punctuated by a predictable migration of mothers away from breeding sites. In contrast, nonmigratory temperate latitude otariid species have a much wider range of lactation periods, with mothers prolonging maternal support in relation to seasonal unpredictability of food resource. Prolonging care into the subsequent reproductive effort will likely have profound effects on the survival of the younger offspring. The Australian sea lion Neophoca cinerea has broken the phylogenetic constraint of a 12-month breeding cycle, which may reflect an alternate strategy to reduce the fitness costs of prolonged support by providing up to 18 months nutritional support to offspring. We use stable isotope analysis of temporally matched whisker sections combined with telemetry data on nutritionally dependent Australian sea lion pups to determine the weaning process and characterize the transition to nutritional independence. Using changes in isotopic nitrogen (δ15N) over time, pups undergo a gradual transition to independent foraging during a 3- to 6-month period before the onset of the next reproductive effort. Telemetry data supported this conclusion, indicating benthic foraging of weaned pups in areas consistent with adult female foraging.

Health assessment of free-ranging endangered Australian sea lion (Neophoca cinerea) pups: Effect of haematophagous parasites on haematological parameters

Evaluation of the health status of free-ranging populations is important for understanding the impact of disease on individuals and on population demography and viability. In this study, haematological reference intervals were developed for free-ranging endangered Australian sea lion (Neophoca cinerea) pups within the context of endemic hookworm (Uncinaria sanguinis) infection and the effects of pathogen, host, and environment factors on the variability of haematological parameters were investigated. Uncinaria sanguinis was identified as an important agent of disease, with infection causing regenerative anaemia, hypoproteinaemia, and a predominantly lymphocytic–eosinophilic systemic inflammatory response. Conversely, the effects of sucking lice (Antarctophthirus microchir) were less apparent and infestation in pups appears unlikely to cause clinical impact. Overall, the effects of U. sanguinis, A. microchir, host factors (standard length, body condition, pup sex, moult status, and presence of lesions), and environment factors (capture-type and year of sampling) accounted for 26–65% of the total variance observed in haematological parameters. Importantly, this study demonstrated that anaemia in neonatal Australian sea lion pups is not solely a benign physiological response to host–environment changes, but largely reflects a significant pathological process. This impact of hookworm infection on pup health has potential implications for the development of foraging and diving behaviour, which would subsequently influence the independent survival of juveniles following weaning. The haematological reference intervals developed in this study can facilitate long-term health surveillance, which is critical for the early recognition of changes in disease impact and to inform conservation management.

Epidemiology of hookworm (Uncinaria sanguinis) infection in free-ranging Australian sea lion (Neophoca cinerea) pups.

Understanding the fundamental factors influencing the epidemiology of wildlife disease is essential to determining the impact of disease on individual health and population dynamics. The host-pathogen-environment relationship of the endangered Australian sea lion (Neophoca cinerea) and the parasitic hookworm, Uncinaria sanguinis, was investigated in neonatal pups during summer and winter breeding seasons at two biogeographically disparate colonies in South Australia. The endemic occurrence of hookworm infection in Australian sea lion pups at these sites was 100% and post-parturient transmammary transmission is likely the predominant route of hookworm infection for pups. The prepatent period for U. sanguinis in Australian sea lion pups was determined to be 11-14 days and the duration of infection approximately 2-3 months. The mean hookworm infection intensity in pups found dead was 2138 ± 552 (n = 86), but a significant relationship between infection intensity and faecal egg count was not identified; infection intensity in live pups could not be estimated from faecal samples. Fluctuations in infection intensity corresponded to oscillations in the magnitude of colony pup mortality, that is, higher infection intensity was significantly associated with higher colony pup mortality and reduced pup body condition. The dynamic interaction between colony, season, and host behaviour is hypothesised to modulate hookworm infection intensity in this species. This study provides a new perspective to understanding the dynamics of otariid hookworm infection and provides evidence that U. sanguinis is a significant agent of disease in Australian sea lion pups and could play a role in population regulation in this species.

Head start: Australian sea lion pups gain experience of adult foraging grounds before weaning

The extended lactation period of the Australian sea lion Neophoca cinerea is suggested to provide additional time for offspring to achieve nutritional independence. We examine the dive and movement development of pups at two age classes (6–10 months) from two colonies (Lilliput and Olive Islands) in South Australia using archival GPS and time-depth recorders to investigate the degree of overlap with maternal home range. Older pups from Lilliput travelled significantly further and spent more time at sea than younger pups. At Olive Island, there was a similar increase in distance travelled and time spent at sea with age. Pups at both colonies started occupying adult female home range at 6 months. Australian sea lion pups can explore adult foraging habitat at least 8 months prior to weaning, allowing them to learn the location of suitable habitat and the skills required to hunt successfully.

Individual identity encoding and environmental constraints in vocal recognition of pups by Australian sea lion mothers

Colonial living imposes strong selection pressures on the communication systems of species with many animals communicating on the same sensory channels simultaneously. Colonial species often exhibit complex individual vocal signatures that encode a caller’s identity in their vocalizations. During lactation, Australian sea lion, Neophoca cinerea, mothers and pups are repeatedly separated when mothers leave the colony to forage. After maternal foraging trips, mothers and pups must reunite in the colony. Both mothers and pups produce individually distinctive vocalizations during reunions and can recognize their counterpart’s calls. Using playback experiments with modified calls, we investigated the acoustic parameters involved in the recognition of pup vocalizations by mothers. We also examined the efficiency of the vocal signature in three habitat types within the colony using propagation tests. We found that Australian sea lion females used a combination of temporal, amplitude and frequency parameters to recognize their pup’s vocalizations. Pup vocalizations were severely degraded in the herbaceous dune habitat type with no vocal signature components reliably propagating to any measured distance. By contrast, calls propagated comparatively well in the shrubby dune habitat of the colony, as the vegetation appeared to act as a windshield. This study shows that the vocal signatures of Australian sea lion pups are both shaped and constrained by their environment and ecology, and that these signatures are of a moderate level of complexity when compared to those of other colonial vertebrates.

Australian sea lions Neophoca cinerea at colonies in South Australia: distribution and abundance, 2004 to 2008

The Australian sea lion Neophoca cinerea is an endemic species listed as vulnerable under the Commonwealth 'Environment Protection and Biodiversity Conservation Act' and as Endangered by IUCN. Assessing its abundance is difficult because of its supra-annual (17 to 18 mo) breeding cycle, and pupping seasons that are extended (about 6 mo but varying between colonies) and asynchronous in their timing between colonies. Based mainly on surveys at most sites in South Australia (SA) between 2004 and 2008, and information from the literature, estimates of abundance are provided for 39 breeding colonies and 9 haulout sites where pups are recorded occasionally. From this study it is estimated that in SA, 3119 Australian sea lion pups are born per breeding cycle, an increase on former estimates by at least 16% resulting from recognition of new breeding colonies, targeting surveys to coincide with maximum pup numbers and using mark-recapture procedures at some colonies. With the addition of 503 pups in Western Australia, the overall estimate of pup abun- dance for the species is 3622. This leads to an estimate of 14 780 animals using the multiplier 4.08. Trend data for the Seal Bay colony on Kangaroo Island indicated that pup numbers decreased at 0.54% yr -1 in the 22 yr (16 pupping seasons) from 1985 to 2007. A cause of the decrease is believed to be bycatch in the demersal shark gillnet fishery, which overlaps with sea lion foraging areas nearby. Area closures declared during 2010 within several km of all Australian sea lion breeding sites in SA should reduce the incidence of bycatch mortality.

Vocal recognition of mothers by Australian sea lion pups: individual signature and environmental constraints

As in all otariids, Australian sea lion, Neophoca cinerea, females alternate foraging trips at sea with suckling periods ashore, and each time they return, mothers and pups have to find each other among individuals at the colony. The need for a finely tuned mechanism of individual recognition is exacerbated by their habit of changing the suckling location. Using playback experiments with modified calls, we investigated the acoustic parameters involved in the discrimination of the mother by pups. The signature efficiency was also tested in the three environments in which reunions at the study site occur by performing propagation tests. Pups paid great attention to both amplitude and frequency modulations, and to the exact frequency values of the call to identify their mother. When severe modifications of AM and FM patterns were made to mothers’ calls pups no longer responded to them. This may have arisen because the calls fell outside the natural species range. The energy spectrum, even though highly individualized, was not important for individual recognition. Propagation tests revealed that one particular environment was extremely harsh and did not allow accurate transfer of the individual signature components whatever the distance. In two other environments, AM was only reliable to a distance of 16 m, but both FM and frequency spectrum could be transmitted with limited degradation over 32 m. The different environments greatly influenced the efficiency of the individual identification process. Accordingly, the area in which mother–pup reunions occur is an important factor in the success of individual recognition.

Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea)

In pinnipeds, maternal care strategies and colony density may influence a species' individual recognition system. We examined the onset of vocal recognition of mothers by Australian sea lion pups (Neophoca cinerea). At 2 months of age, pups responded significantly more to the calls of their own mothers than alien female calls demonstrating a finely tuned recognition system. However, newborn pups did not respond differentially to the calls of their mother from alien female calls suggesting that vocal recognition had not yet developed or is not yet expressed. These findings are in stark contrast to other otariid species where pups learn their mother's voice before their first separation. Variance in colony density, pup movements, and natal site fidelity may have reduced selective pressures on call recognition in young sea lions, or alternatively, another sensory system may be used for recognition in the early stage of life.