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Hookworm Infection in the Australian Sea Lion

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Hookworm Infection in the Australian Sea Lion Hookworm infection in the Australian sea lion (Neophoca cinerea) Alan David Marcus A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Faculty of Veterinary Science The University of Sydney 2015 Statement of authentication This thesis is submitted to the University of Sydney in fulfilment of the requirements for the degree of Doctor of Philosophy. The work presented in this thesis is, to the best of my knowledge and belief, original except as acknowledged in the text. I hereby declare that I have not submitted this material, either in full or in part, for a degree at this or any other institution. Alan David Marcus June 2015 i Summary of the thesis Parasites are integral components of biodiverse ecosystems and profoundly impact the health and population dynamics of many free-ranging species. The sequelae of parasitic infection fluctuate along a continuum from beneficial to detrimental host effects, mediated by the dynamic interaction of host, pathogen, and environment factors. Understanding the effects of parasitic infection, and the fundamental factors influencing the epidemiology of disease, is essential to determining the need for, and approach to, control strategies to conserve complex ecosystems. For the Australian sea lion (Neophoca cinerea), an endangered keystone predator that demonstrates high rates of pup mortality and limited population recovery, an understanding of the role of infectious disease in influencing pup health, and how it may contribute towards shaping population demography, is a key knowledge gap. Preliminary investigations indicated that hookworm (Uncinaria sp.) infection is an important cause of disease and mortality in Australian sea lion pups. These findings were the impetus for this thesis to investigate the taxonomy, epidemiology, clinical impact, and management of hookworm infection in the Australian sea lion. Chapter 1 of this thesis describes the natural history of the Australian sea lion and outlines the key threats and knowledge gaps pertaining to the species’ survival. The state of knowledge regarding hookworm infection in pinnipeds is reviewed and the aims of this thesis are presented. Field work for this study was undertaken at two major colonies of the Australian sea lion in South Australia – Seal Bay, Kangaroo Island, and Dangerous Reef, Spencer Gulf – during consecutive breeding seasons in 2010–2013. These colonies were selected primarily for their disparate biogeographical features and opposite seasonal patterns of variation in pup mortality, facilitating investigation of the role of host, pathogen, and ii environment factors in influencing the epidemiology and clinical impact of hookworm infection in this species. Hookworms collected from Australian sea lion pups were identified and described in Chapter 2 as a single, novel species (Uncinaria sanguinis). Substantial inter-host morphometric variation in both juvenile and adult specimens of U. sanguinis was identified, demonstrating the limited utility of quantitative morphometrics to discriminate between different Uncinaria species, which engenders caution when delimiting new species. However, morphological features and differences in nuclear ribosomal DNA sequences clearly delineated U. sanguinis from named congeners. By determining the taxonomic identity of hookworms parasitising Australian sea lion pups, this study provided a solid foundation to investigate the epidemiology, clinical impact, and management of this parasite. Findings presented in Chapters 2, 3, and 5 indicate that, as for hookworm infection in other otariid species, transmammary transmission in the immediate post-parturient period is likely the predominant route leading to patent hookworm infection in Australian sea lion pups. However, in contrast to the fundamental role that colony substrate appears to play in shaping the epidemiology of hookworm infection in these other hosts, the findings of Chapter 3 demonstrate that 100 % of Australian sea lion pups are infected with U. sanguinis irrespective of the type of colony substrate, and that the intensity of hookworm infection (mean intensity of 2138 hookworms per pup) appears to be influenced by colony- specific seasonal differences in host behaviour. Seasonal fluctuations in the intensity of hookworm infection corresponded to oscillations in the magnitude of colony pup mortality; higher hookworm infection intensity was associated with higher colony pup mortality as well as reduced pup body condition. This study implicates U. sanguinis as a key factor shaping the population demography of the Australian sea lion and provides a new iii perspective to understanding the fundamental factors that influence the dynamics of hookworm infection in otariids. Chapter 4 of this thesis improves the understanding of the impact of infectious disease on the health status of Australian sea lion pups by estimating the effects of pathogen, host, and environment factors on the values of haematological parameters. In addition, haematological reference intervals were developed for free-ranging Australian sea lion pups within the context of endemic hookworm infection to facilitate health assessment. Uncinaria sanguinis was identified as a significant agent of disease, with infection causing regenerative anaemia, hypoproteinaemia, and a predominantly lymphocytic-eosinophilic systemic inflammatory response. Further evidence that U. sanguinis causes intensity-dependent disease in pups was provided by the findings of higher eosinophil counts and lower total plasma protein values during high hookworm infection intensity seasons compared to low hookworm infection intensity seasons at both colonies. Interestingly, the degree of eosinophilia observed in this study was markedly higher than that previously reported for other otariid pups, possibly reflective of the higher intensity and pathogenicity of hookworm infection in Australian sea lion pups. This study demonstrated the significant adverse impact that U. sanguinis has on the health status of Australian sea lion pups and, by demonstrating that the occurrence of neonatal anaemia is not solely a benign physiological response to host-environment changes in this species, challenges assumptions about the non-pathological nature of neonatal anaemia in other pinnipeds. Chapter 4 also presents findings on the epidemiology and clinical impact of sucking lice (Antarctophthirus microchir) infestation in Australian sea lion pups. This parasite was identified commonly on pups (> 70 % prevalence) but, in contrast to hookworm infection, the clinical impact of infestation was less severe, associated only with mild anaemia and iv hyperproteinaemia, and is considered unlikely to be having a significant impact on the health status of Australian sea lion pups. In addition, findings in Chapters 4 and 5 indicate that the prevalence and intensity of lice infestation may increase secondary to hookworm infection, suggesting that some of the effects attributed to A. microchir are correlatively, rather than causatively, associated with their occurrence. Chapter 5 reports the results of investigations at Dangerous Reef to test the association of U. sanguinis with disease in Australian sea lion pups by experimentally manipulating the host-parasite relationship via anthelmintic administration. Ivermectin was found to be highly effective (97.9 %) at eliminating U. sanguinis from pups and was also effective (91.4 %) at removing A. microchir for up to 2 months. As such, it was not possible to definitively distinguish between the independent effects of these parasites, however, given that U. sanguinis was otherwise identified to have greater pathological impact than A. microchir, it is likely that the changes observed in clinical parameters in treated pups were predominantly due to the elimination of hookworm infection. Pups administered ivermectin had significantly higher erythrocyte counts and significantly lower eosinophil counts relative to saline-treated control pups at 1–2 months post-treatment. Unexpectedly, ivermectin treatment was not significantly associated with beneficial effects on pup growth and survival, highlighting the challenges associated with treating pups of this species shortly after birth at a remote colony. This study contributes towards understanding the utility of anthelmintic treatment as a tool for the conservation management of free-ranging wildlife and outlines essential steps to further the development of strategies to ensure the effective conservation of the Australian sea lion and its parasitic fauna. Chapter 6 discusses the significance of the major findings of the studies in this thesis and their implications for the conservation management of the Australian sea lion. v Limitations of the studies are also discussed and directions for future research are proposed. The baseline epidemiological data and the haematological reference intervals described in this thesis can facilitate the implementation of long-term health surveillance in this species, which is critical for the early recognition of emerging disease and changes in disease impact so that interventional strategies can be implemented. This thesis determined that U. sanguinis is an important cause of disease in the Australian sea lion and implicated this parasite as a major factor contributing towards pup mortality. As such, this body of work contributes towards an improved understanding of the role of infectious disease in influencing the health status and population demography of this endangered
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