The biology of the cosmopolitan fish parasite Neobenedenia girellae

Brazenor, Alexander Karlis (2017) The biology of the cosmopolitan fish parasite Neobenedenia girellae. PhD thesis, James Cook University.

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Monogeneans are a fascinating parasite group to study. They can be harmful pathogens of finfish and display interesting relationships with their hosts making research on these species engaging from both ecological and economic perspectives. Neobenedenia (Family Capsalidae) Yamaguti, 1963, is a notable monogenean genus and is notorious for the large number of potential host species that the constituent parasite taxa are able to infect. The distinct lack of research on Neobenedenia biology and the diversity of species present in Australian waters presented me with an opportunity to conduct a series of research studies designed to improve understanding of this parasite genus. The aim of this thesis was to provide an in-depth investigation of Neobenedenia phylogenetics and detailed biology (including the growth, morphology, reproduction, and biochemistry) of the species in Australia.

The first data chapter (Chapter 2) determined the phylogenetic relationships between 33 Neobenedenia isolates by amplifying three genes; two nuclear (H3 and 28S rDNA) and one mitochondrial (cytochrome b). Isolates were collected from a total of 23 host species and nine countries in both hemispheres and included 16 isolates from 12 host fishes in Australia. Representative samples for Neobenedenia melleni MacCallum, 1927, Neobenedenia pacifica Bravo-Hollis, 1971, and Neobenedenia longiprostata Bravo-Hollis, 1971, formed discrete clades and collectively accounted for seven of the 33 samples used in this study. The remaining 26 isolates formed a single clade genetically distinct from all representative specimens. Morphological observation of these 26 isolates confirmed that they were morphologically indistinguishable from N. melleni despite displaying clear genetic differences in the phylogenetic trees. This confirmed the suggestion by the scientific community that Neobenedenia girellae Hargis, 1955, a species that was synonymised with N. melleni in 1996, should be reinstated as its own taxon, a recommendation that is encouraged by the authors.

The second data chapter (Chapter 3) focussed on the effect that a number of environmental variables had on the morphology of N. girellae. Neobenedenia girellae is extremely flexible in the morphology it exhibits. Temperature was identified as the strongest factor affecting the morphology of this species, however, there was an indication that morphology may also be dictated by the host species that the parasite attaches to. Between different host species, parasites exhibited changes in the morphology of the attachment organs which come in direct contact with their host's surface. This is proposed to be a function of maximising the ability of their attachment organs to the scale/mucus interface of heterogeneous host surfaces. The morphology of parasites attached to the same host species at different temperatures differed most in their total body size. Features associated with the attachment of the parasite to the host did not differ which is likely a product of the homogenous host surface available to the parasite. The variation observed in this species explains why N. melleni and N. girellae have been misidentified, fuelling considerable taxonomic confusion in Neobenedenia in the past.

The third data chapter (Chapter 4) focussed on elucidating reproductive and life cycle biology of N. girellae in temperatures and salinities typical of tropical regions. Neobenedenia girellae completed its life cycle almost twice as fast in warm, high saline conditions compared to cooler temperatures. Hatching and infection success and oncomiracidia longevity was significantly reduced in salinities less than 22 ‰ compared to higher saline conditions (35 and 40 ‰). A total of two strategically timed treatments on stock was recommended in cool to moderate temperatures in salinities of seawater or higher. In warmer conditions (> 30 ºC), a third treatment of stock is required as parasites reach sexual maturity faster than the time taken for all eggs to hatch in a given period. The development of an accessible and user-friendly strategic treatment timetable informs fish farmers and aquarists alike when to treat their fish to maximise the efficacy of treatments and minimise labour costs and reinfection.

The fourth data chapter investigated the feasibility of collecting sufficient quantities of N. girellae eggs for biochemical analysis (Chapter 5). An established laboratory culture of N. girellae was optimised to enable the production of larger quantities of eggs over short periods of time for collection and subsequent biochemical analysis. Eggs were found to be composed primarily of water (79.12 %) followed by protein (11.51 %) and lipid (2.50 %). Lipids were composed of approximately equal amounts of saturated, monounsaturated, and polyunsaturated fatty acids (35.43 ± 0.38 %, 29.08 ± 0.38 %, and 35.50 ± 0.53 %, respectively). The predominant lipid classes were phosphatidylcholine (21.90 ± 1.42 %) and triacylglycerols (TAG) (33.82 ± 1.20 %). This is the first study to quantify the biochemical components of marine monogenean eggs but only provided insight into the biochemical contents of N. girellae eggs after they had been laid and not throughout development.

Chapter 6 expanded on the topics identified in Chapter 5 and quantified the biochemical contents of eggs throughout embryogenic development and across a range of temperatures. This provided valuable information on metabolic fuels employed by embryos as they developed and in different environments. Additionally, reproductive biology (fecundity, egg-laying period, and egg volume) was investigated to provide a complete picture of N. girellae reproductive investment. Adult parasites were significantly larger at cooler temperatures and produced significantly larger eggs towards the end of their reproductive lives. Fecundity of adults was highest at 20 and 30 ºC compared to 25 ºC. The biochemistry of freshly laid eggs was similar to the results observed in Chapter 5. Proximate composition of eggs did not significantly change over the three temperatures tested, however, warmer temperatures resulted in the significant decrease in a number of mono- and polyunsaturated fatty acids throughout embryogenesis. The most prolific lipid classes were phospholipids and TAGs. The most notable change from the biochemical profile observed in Chapter 5 was that the amount of acetone mobile polar lipids in eggs more than doubled in the present study to compose up to 25% of the lipids in N. girellae eggs.

Neobenedenia girellae is a parasite with a turbulent taxonomic history. Now that appropriate genes have been recognised that can accurately identify this species, potentially misidentified samples from previous studies can be clarified and the geographic and host records can be built on a solid foundation. This allows for future research to confidently credit any biological research to this taxon which has important implications for modelling populations on hosts, epidemiology, and management of this species on dozens of host taxa. If, as predicted, parasites and pathogens become a more immediate problem for global food security in a rapidly changing climate, accurately defining and identifying threats and developing methods for management and eradication of these species is paramount. This thesis presents a comprehensive assessment of one of the most cosmopolitan monogenean species in the world and the intimate knowledge generated on its biology can be used to reduce the impact of outbreaks on food fish production.

Item ID: 52681
Item Type: Thesis (PhD)
Keywords: aquaculture, Asian sea bass, biochemistry, Capsalidae, cryptic species, egg hatching, lipid, Monogenea, natural selection, Neobenedenia, phenotypic plasticity, Platyhelminthes, protein, skin fluke, treatment
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 3: Brazenor, Alexander K., Saunders, Richard J., Miller, Terrance L., and Hutson, Kate S. (2018) Morphological variation in the cosmopolitan fish parasite Neobenedenia girellae (Capsalidae: Monogenea). International Journal for Parasitology, 48 (2). pp. 125-134.

Chapter 4: Brazenor, Alexander K., and Hutson, Kate S. (2015) Effects of temperature and salinity on the life cycle of Neobenedenia sp. (Monogenea: Capsalidae) infecting farmed barramundi (Lates calcarifer ). Parasitology Research, 114 (5). pp. 1875-1886.

Chapter 5: Brazenor, Alexander K., Francis, David S., Hutson, Kate S., and Carton, Alexander G. (2017) Biochemical composition of marine monogenean parasite eggs. Molecular and Biochemical Parasitology, 218. pp. 1-3.

Date Deposited: 26 Feb 2018 04:24
FoR Codes: 07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070404 Fish Pests and Diseases @ 100%
SEO Codes: 96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960407 Control of Pests, Diseases and Exotic Species in Marine Environments @ 50%
96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960402 Control of Animal Pests, Diseases and Exotic Species in Coastal and Estuarine Environments @ 50%
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