Jones, Karina (2019) Environmental influences on the epidemiology of fibropapillomatosis in green turtles (Chelonia mydas) and consequences for management of inshore areas of the Great Barrier Reef. PhD thesis, James Cook University.

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Abstract

The epidemiology of fibropapillomatosis (FP) in marine turtles is a global conservation concern and, until now, there has been a paucity of data surrounding this disease in Australia. An understanding of FP is critical to the effective management of all marine turtles, but particularly the endangered green turtle (Chelonia mydas) as this species is predominantly affected by FP. Green turtles have a complex life-history which includes a high degree of site fidelity; once recruited into a foraging area turtles will typically remain there, despite damage or destruction to their habitat. It is this trait, coupled with their long-lived nature, that has led them to be recognised as sentinels of marine ecosystem health; this species is particularly susceptible to the detrimental effects of environmental change. With high prevalence of FP consistently linked to regions associated with reduced water quality, the relationship between this disease and the environment is of increasing interest. A herpesvirus (chelonid alphaherpesvirus 5; ChHV5) has been identified as the likely aetiological agent of this disease. The distribution of variants of this virus appear to differ by region, indicating a sitespecific element to viral transmission. These elements of the disease highlight the need for investigation of FP, ChHV5 and the environmental factors which may be facilitating disease manifestation in all regions where this disease has been reported.

The overarching aim of this thesis was to address the information gap for FP in green turtles in Australian waters and to provide recommendations for management of inshore areas of the GBR. This thesis clarified the spatial distribution and prevalence of FP along the Queensland coast, which encompasses the Great Barrier Reef (GBR). A potential relationship between FP prevalence and water quality on the GBR was also evaluated. To test for horizontal or vertical transmission of chelonid alphaherpesvirus 5 (ChHV5), a relationship between host genetic stock and viral variant was also investigated. Both inshore and offshore sites were studied throughout the thesis, yet the inshore study sites are under a greater influence of water that originates from the adjacent catchment; flood plumes rarely extend further than mid-shelf reefs and non-flood river outflow almost exclusively affects inshore areas. As such, the focus of this thesis is on the inshore areas of the GBR.

This thesis provides the first comprehensive report of FP prevalence in Australia. The spatial distribution and prevalence of FP on the GBR was characterised using 25,645 records from 15 sites along the Queensland coast. A total of 791 turtles with FP tumours were recorded in this dataset. The results of this study show that FP prevalence varies between sites and years, with juvenile turtles being the most frequently affected by FP. Survey method had a significant influence on the apparent FP prevalence value at each site; surveys which explicitly targeted FP detected higher numbers of individual turtles with FP and therefore generated higher prevalence rates than general population surveys. This study highlighted shortcomings in both methods with respect to FP detection, and this must be considered when interpreting results and developing future marine turtle surveys.

A relationship between a subset of this FP prevalence data and water quality at these sites was assessed using water quality indices (WQIs). Sub-indexes for dissolved inorganic nitrogen (DIN), total suspended solids (TSS), pesticides and metals were developed for each study site using published data from a range of sources and enhanced using expert opinion. These WQI scores were also aggregated without weights to create an overall water quality index for each study site. A total of 18,380 records of individual capture records of green turtles, including 264 records of FP across 14 sites along the GBR, were used in conjunction with the WQIs. Despite the analysis of this expansive dataset, a significant relationship between FP prevalence and WQI rankings at each site could not be quantified or established. This investigation is the first attempt at creating WQIs based on data from published reports and peer-reviewed publications to compare with FP prevalence data along the Queensland coast. Unfortunately, due to the different methods used to capture and record data this information could not be used as 'fit-for-purpose' and it proved impossible to bridge between differing methods. However, this result does have significant implications for management as it highlights the importance of designing water quality monitoring programs and data capture in the GBR so these can be used across multiple disciplines in a more integrated way.

It has long been postulated that turtles first encounter the infectious agent of FP through horizontal transmission at their foraging grounds, and reports of the site-specific distribution of ChHV5 variants appear to support this theory. However, this theory has never been assessed by studying the genetic origin of the host turtle. Turtles frequenting a given foraging site usually represent genetic stock from multiple rookeries, with genetic stocks reflecting the region of origin. For example, turtles originating from rookeries in the southern GBR are genetically similar, yet genetically distinct from those originating from rookeries in the northern GBR. If ChHV5 transmission was occurring vertically from parent to offspring, then phylogenetic clustering of ChHV5 would be expected to be based on host genetic stock, rather than on sampling location. Conversely, if ChHV5 transmission is occurring horizontally at foraging grounds, a link between viral variant and host origin would be less likely.

To facilitate an investigation of host genetic origin and the ChHV5 variant each turtle was infected with, we first developed an assay which targets a longer fragment of mitochondrial DNA than used in previous studies. This assay was validated through a mixed stock analysis (MSA) of 278 turtles across three foraging grounds spanning more than 330 km: Cockle Bay, Green Island and Low Isles. The MSA utilised the mtDNA sequences generated in this study to estimate the relative proportion of genetically-distinct breeding populations found at each foraging ground. Haplotype and nucleotide diversity was also assessed. A total of 35 haplotypes were identified across all sites, 13 of which had not been found previously in any rookery. The results showed that the northern GBR (nGBR), Coral Sea (CS), southern GBR (sGBR) and New Caledonia (NC) stocks supplied the bulk of the turtles at all three sites, with small contributions from other rookeries in the region. Stock contribution shifted gradually from north to south, although sGBR/CS stock dominated at all three sites. The major change in composition occurred between Cockle Bay and Low Isles. Our findings, together with other recent studies in this field, show that stock composition shifts with latitude as a natural progression along a coastal gradient. This phenomenon is likely to be the result of ocean currents influencing both post-hatchling dispersal and subsequent juvenile recruitment to diverse coastal foraging sites.

In addition to serving as a method validation, the results of the MSA improved our knowledge of the spatial ecology of green turtles on the GBR, which is fundamental to their effective conservation. The findings from this study were then combined with those of previous studies to provide a tool to estimate the main relative stock contributions at as yet unsampled foraging grounds. Such a tool may allow managers to target their efforts more effectively.

Following the development of the mtDNA assay for identification of host genetic origin, a relationship between host genetic origin and ChHV5 variant was investigated. This thesis presents improved molecular assays developed for detection of ChHV5, in combination with a robust molecular and phylogenetic analysis of ChHV5 variants. This approach utilised a multi-gene assay to detect ChHV5 in all FP tumors sampled from 62 marine turtles found at six foraging grounds along the Great Barrier Reef. Six distinct variants of ChHV5 were identified and the distribution of these variants was associated with host foraging ground. However, no association between host genetic origin and ChHV5 viral variant was found. These findings support the hypothesis that marine turtles undergo horizontal transmission of ChHV5 at foraging grounds and are unlikely to be contracting the disease at rookeries, either during mating or vertically from parent to offspring. As a consequence, management of this disease should be focused on green turtle foraging grounds.

Item ID:	64591
Item Type:	Thesis (PhD)
Keywords:	chelonid herpesvirus 5, conservation biology, fibropapillomatosis, green turtle, herpesvirus, marine biology, marine turtle, molecular biology, natural resource management, population biology
Related URLs:	https://researchonline.jcu.edu.au/42105/ https://researchonline.jcu.edu.au/56614/ https://researchonline.jcu.edu.au/61391/
Copyright Information:	Copyright © 2019 Karina Jones.
Additional Information:	Three publications arising from this thesis are stored in ResearchOnline@JCU, at the time of processing. Please see the Related URLs. The publications are: Chapter 2: Jones, K., Ariel, E., Burgess, G., and Read, M. (2016) A review of fibropapillomatosis in green turtles (Chelonia mydas). The Veterinary Journal, 212. pp. 48-57. Chapter 5: Jones, Karina, Jensen, Michael, Burgess, Graham, Leonhardt, Johanna, van Herwerden, Lynne, Hazel, Julia, Hamann, Mark, Bell, Ian, and Ariel, Ellen (2018) Closing the gap: mixed stock analysis of three foraging populations of green turtles (Chelonia mydas) on the Great Barrier Reef. PeerJ, 6. 5651. Chapter 6: Jones, K., Burgess, G., Budd, A.M., Huerlimann, R., Mashkour, N., and Ariel, E. (2020) Molecular evidence for horizontal transmission of chelonid alphaherpesvirus 5 at green turtle (Chelonia mydas) foraging grounds in Queensland, Australia. PLoS ONE, 15 (1). e0227268.
Date Deposited:	15 Oct 2020 00:01
FoR Codes:	07 AGRICULTURAL AND VETERINARY SCIENCES > 0707 Veterinary Sciences > 070712 Veterinary Virology @ 34% 07 AGRICULTURAL AND VETERINARY SCIENCES > 0707 Veterinary Sciences > 070704 Veterinary Epidemiology @ 33% 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060412 Quantitative Genetics (incl Disease and Trait Mapping Genetics) @ 33%
SEO Codes:	96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960407 Control of Pests, Diseases and Exotic Species in Marine Environments @ 34% 96 ENVIRONMENT > 9605 Ecosystem Assessment and Management > 960503 Ecosystem Assessment and Management of Coastal and Estuarine Environments @ 33% 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 33%
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