Aquaculture and Fisheries Development Centre – Doctoral Theses

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Cockle health, disease connectivity and trophic interaction dynamics
(University College Cork, 2021-11-30) Albuixech-Martí, Sara; Culloty, Sarah C.; Lynch, Sharon A.; European Regional Development Fund
Parasites and pathogens are an essential part of the community structure, and their transmission and development are affected not only by their host’s immune system and host population density, but also by multiple biological and environmental drivers that impact on the host-parasite dynamics. There are many gaps in the understanding of these processes and how they influence one another. Given their ecological and economic importance and their exposure to fluctuating and stressful coastal environments, common cockles Cerastoderma edule are ideal model organisms to investigate these dynamics within a natural framework. Therefore, this thesis is intended to present C. edule as a model pathosystem to study marine epizootics and their increased risk of occurrence due to the current changing environment. This thesis develops the understanding of the biological and environmental factors that influence the distribution and dynamics of the host-parasite interplay. In this study, single and multiple parasite and pathogen infections plus over a range of study areas were utilised to better understand these dynamics. The initial part of the study describes a previously undocumented geographic range on the northeast and south coasts of Ireland of two haplosporidian species, Minchinia tapetis and Minchinia mercenariae-like, that have been recently characterised in C. edule. In order to understand the Minchinia:cockle disease dynamics, species-specific primers were developed and these parasites were detected by PCR and confirmed by sequencing. The histology, in turn, confirmed the presence of spore-like stages in the connective tissues of C. edule. A range of factors including host condition and environmental drivers affected both spatial and temporal patterns of these haplosporidian infections in C. edule. Based on statistical modelling, high dissolved oxygen in seawater and small cockle size were the main drivers of the haplosporidian prevalence in the study. The detailed examination of a wider microbial community within C. edule by PCR and histology revealed that single infections with Haplosporidia or Vibrio were more common than coinfected individuals, as expected by random chance. During this second study, no microsporidian species nor ostreid herpesvirus-1 microVar (OsHV-1 μVar) or variants were detected. Based on statistical modelling, coinfected individuals with Haplosporidia and Vibrio occurred because the same risk factors (increased seawater temperature, reduced salinity, and poor host condition) promoted their presence and increased the probability of infection by both pathogen groups. Coinfection with both Minchinia species was overrepresented in our samples and a positive association between M. tapetis and M. mercenariae-like was statistically confirmed. Findings emphasise the need for a more holistic approach in pathological studies, considering the diverse pathogen community within the cockle and their relationship with the environment. The transmission of the microbial community within C. edule to shorebird populations via consumption of cockles and the existing connectivity with the environment (sediment) were also assessed by molecular techniques (PCR and Sanger sequencing) during a third study. Identical strains of Vibrio splendidus were identified in C. edule and, for the first time, in shorebird faecal samples. The consumption of C. edule, thus, may be a source of this Vibrio species in shorebirds. Our findings add evidence to the significant role migratory birds may have as carriers of infectious agents, enabling their transport and dispersal. The findings also support the role of the sediment as an environmental reservoir for Vibrio, which may have an impact on the infaunal community within the sediment responsible for different ecosystem services. Ultimately, in a study that spanned the east and west coast of Ireland and the Welsh coast, patterns of occurrence of Minchinia and Vibrio spp. in C. edule were associated with environmental stressors (high concentration of nitrates and warm temperatures), which may have affected host susceptibility and increased pathogen prevalence. These findings highlight the impact of site-specific environmental stress and habitat degradation on pathogen emergence, particularly in coastal marine environments. In conclusion, this thesis develops a greater understanding of C. edule as a pathosystem and its potential for the early detection of emergent infectious agents, which will have important implications for the sustainability of wild and cultured bivalve populations and the functioning of coastal ecosystems in a changing environmental context.
Invasive species and aquaculture pathogens in the Irish and Celtic Seas
(University College Cork, 2021-04-01) Costello, Katie Ellen; Culloty, Sarah C.; Lynch, Sharon A.; Mcallen, Robert; Ramsay, Ruth; European Regional Development Fund
Invasive species represent a major threat to biodiversity and ecosystem functioning, however research into the interactions between invasive species and their parasites is lagging far behind research into general invasion biology. This thesis explores the relationship between invasive species, specifically those which impact the aquaculture sector through biofouling or predation on commercial species, and the parasites and pathogens with which they interact. Focus is paid to bivalve aquaculture, since species such as the Pacific cupped oyster Crassostrea gigas and the blue mussel Mytilus edulis are heavily cultured within the study regions. The first research chapter takes the form of a review which synthesises invasive host-parasite interactions using marine bivalves as a model group. The global aquaculture industry is discussed in detail, as often it is this industry that facilitates the spread of both invasive species and disease, but it is also this industry that is adversely impacted by subsequent disease outbreaks. The chapter then provides recommendations to enhance our understanding of marine diseases, and also addresses how climate change might influence invasive host-parasite complexes. The second data chapter investigates the impact of one particular group of invasive species - tunicates that can have a significant impact on aquaculture. The study looks at the impact of these tunicates on the maintenance of select pathogens that affect commercial bivalves, including the ostreid herpesvirus OsHV-1 μVar, the bacterium Vibrio aestuarianus and the haplosporidia Bonamia ostreae and Minchinia spp. PCR, Sanger sequencing and histology confirmed the presence of B. ostreae and Minchinia mercenariae-like in the leathery/club tunicate Styela clava, and V. aestuarianus was confirmed by qPCR in the orange sheath tunicate Botrylloides violaceus and the carpet sea squirt Didemnum vexillum. Furthermore, histology confirmed M. mercenariae-like sporonts in S. clava suggesting that the tunicate can facilitate replication of this species. The results indicate that tunicates can act as reservoirs of infection in areas where disease occurs and potentially transport diseases to uninfected sites. Microbial diversity in nearshore bivalve culture environments is well-documented, but less is known about offshore environments. The third data chapter of this thesis examined 65 plankton samples collected from the Irish and Celtic Seas in May 2018 to investigate zooplankton-associated microbial communities. Bacteriome sequencing was used to characterise the bacterial community structure and identify any potential pathogens, and PCR was also used to further screen for haplosporidian and viral pathogens. The bacterium Vibrio splendidus was detected, as was a haplosporidian species (18_Haplo_BMVA_WEY) first detected off Weymouth, England between 2011-2012. The results also revealed distinct bacterial profiles arising from the Irish Sea, Celtic Front, Eastern Celtic and Southern Celtic Sea areas, suggesting that oceanic currents and fronts may act as barriers or facilitators to microbial dispersal thereby providing pathways for pathogens. The final empirical chapter of this thesis takes the form of a horizon scanning exercise utilising cargo shipping records from 2018-2019 (n = 9,291). The chapter focuses on the connectivity between four major ports in Ireland (Dublin, Cork, Rosslare and New Ross) and global shipping ports. Ballast water and hull fouling are vectors for invasive species movements, and regional management may be strengthened by identifying shipping networks as this will allow for targeted inspections. A targeted horizon scanning exercise for invasive species likely to arrive in Ireland was included, and seventeen incoming ports were highlighted as having high connectivity to Ireland. Furthermore, the focal invasive species are present in these ports, suggesting there is strong potential for invasion. Shipping routes within Ireland also demonstrate high connectivity, meaning the potential for secondary spread is strong. The thesis concludes with a discussion highlighting the main findings and emphasising the importance of integrating the fields of parasitology and invasion ecology to enhance our understanding of pathogen dispersal and transmission.
A temporal investigation of Europe-wide drivers of cockle Cerastoderma edule biology, health and population dynamics
(University College Cork, 2020-12) Mahony, Kate Ellen; Culloty, Sarah C.; Lynch, Sharon A.; European Regional Development Fund
The common cockle Cerastoderma edule is an economically, ecologically and culturally important bivalve species and provides a range of ecosystem services. However, increasing reports of cockle mass mortalities, coinciding with reduced harvests, are a concern for various stakeholders. The factors responsible for these mass mortalities (e.g. parasites, weather extremes) are likely to be exacerbated by climate change, making it necessary to examine past and present trends in cockle biology, in order to make plans for the future protection of this species. To examine the key drivers of cockle populations, historic analysis and current field surveys were conducted. Historic data were collated to understand past trends of abundance, spawning and harvesting, at both a local and global scale. The current impact of biotic (parasites) and abiotic (latitude, environment and fishing) factors on cockle populations were investigated in a 19-month survey. This field study was conducted across latitudinally varying European sites (Ireland to Portugal) and combined histological techniques and morphometric analysis to examine gametogenesis, health and growth, and the key biotic and abiotic modulators of these characteristics. The evident trends were then considered in the context of future climate change. The variability in cockle populations was affirmed, particularly at a local scale. At a global scale, climate was found to historically influence cockle populations, with warmer waters resulting in reduced abundance. However, historic data collection was lacking in coordination across borders and between stakeholders. The current study, which was more coordinated, also demonstrated the potential influence of climate. In terms of reproduction, cockles at warmer southern sites exhibited prolonged spawning. Additionally, growth was found to be reduced at warmer temperatures, likely due to a diversion of energy to gametogenesis. This highlights a potential impact on the growth and spawning of northern cockles as a result of climate change. Furthermore, trematodes (both metacercariae and sporocysts) were found to negatively impact gametogenesis and growth. Previous studies highlighted the influence of climate change on increased trematode transmission, and this was supported in this thesis, with increased sporocyst prevalence linked with warmer water. Furthermore, additional information was discovered relating to the potential influence of climate change on a range of mortality inducing parasites (e.g. bacteria, Trichodina ciliates, sporocysts, metacercariae), which are likely to increase as a result of the previously predicted warming seas and increased precipitation. The results presented in this thesis have a number of implications for the protection of cockles and ensuring future sustainability of European populations. In particular, regular monitoring at a local scale is necessary, due to the evident micro-variability of cockle population characteristics. This regular monitoring, in particular of reproduction and growth rates, was shown to be necessary in creating management strategies, in particular for setting minimum harvest size. A lack of data mobility was noted between scientists, managers, conservationists and the public, highlighting the necessity of data sharing efforts not just for cockles, but for all commercially exploited species. Finally, climate change is evidently a major threat to cockles, however this study and the future resulting research, which has been widely disseminated to a variety of stakeholders, will assist the protection of the common cockle.
Improving the sustainability of aquaculture: investigating novel experimental concepts and techniques
(University College Cork, 2017) Gunning, Daryl; Sullivan, Timothy; Burnell, Gavin; Maguire, Julie; Irish Research Council
The overall aim of this thesis is to investigate novel concepts and techniques that have the potential to improve the sustainability of the marine aquaculture industry. The focus of the research described here is on novel ecosystem approaches to aquaculture management by integrating species from multiple trophic levels into one system. This has been termed Integrated Multi-Trophic Aquaculture (IMTA), a concept that combines (ideally, in the appropriate proportions) the cultivation of fed aquaculture species (e.g. finfish or shrimp), with organic and inorganic extractive species (e.g. bivalve molluscs, seaweed or halophytes). Emphasis throughout has been placed on improving techniques and novel concepts that have the potential to be of practical sustainable use to existing and future industrial aquaculture operations. Chapter 1 specifically details the development of sustainable saltwater-based food production systems, with a focus on established and emerging concepts. In Chapter 2, the biofiltering capacity of the halophyte Salicornia europaea is assessed, with a focus on biofiltering capacity when irrigated with wastewater from an oyster hatchery and cultivated via the novel hydroponic techniques. In Chapter 3, the efficacy of different stratification methodologies on S. europaea seed germination and growth are assessed, while Chapter 4 deals with the effectiveness of three anaesthetics in reducing error when measuring the size of cotton-spinner sea cucumber Holothuria forskali. The efficacy of passive integrated transponder (PIT) tags for H. forskali are assessed in Chapter 5 and Chapter 6 describes the cultivation of six species of seaweed in small-scale zero exchange maraponic systems with blue mussels (Mytilus edulis), Japanese abalone (Haliotis discus hannai) and Holothuria forskali. Finally, Chapter 7 details practical considerations and theoretical aspects of set-up and operation of a pilot-scale IMTA system (seaweed longlines containing Alaria esculenta and Saccharina latissima) in conjunction with a commercial organic salmon farm in Southern Ireland.
The role of intrinsic and extrinsic factors in shaping alternative migratory tactics and metabolic phenotypes in brown trout
(University College Cork, 2019-11) Archer, Louise C.; Reed, Thomas; Mcginnity, Philip; European Research Council
Variation among and within populations accounts for a considerable portion of phenotypic diversity produced in nature, and is instrumental to the structure and function of ecosystems. Understanding how, and why, intraspecific diversity persists is essential for predicting and managing the effects of global change, particularly because intraspecific variation may mediate diverse responses to changes in the environment. Alternative phenotypes – i.e. discrete phenotypic variation – can arise from a combination of proximate and ultimate mechanisms. Proximate mechanisms reflect how environmental factors shape phenotypic variation via intermediate physiological processes, which can themselves vary and be decomposed into genetic versus environmental components. Ultimate mechanisms concern the evolutionary function of a given phenotype. In this thesis, I explore how proximate and ultimate factors contribute to a particularly striking example of intraspecific diversity: alternative migratory tactics in brown trout Salmo trutta. Brown trout are iconic for the variety of migratory life histories they exhibit; yet fundamental knowledge gaps remain regarding how environmental, physiological, and genetic factors integrate to underpin life history decisions among and within populations. In Chapter 2, I assessed how food restriction and population background influences the expression of migratory tactics in offspring from two populations that naturally differ in anadromy (i.e. sea-migration). Food restriction affected traits related to size and condition, and resulted in a higher frequency of anadromy in both populations, though populations varied in their responses according to the timing of food restriction treatments. While anadromy was overall more frequent in offspring from the naturally anadromous population, the expression of anadromous phenotypes in offspring from a non-anadromous population indicated that migratory tactics might emerge in response to unfavourable environmental conditions causing energetic limitation. In Chapter 3, I further considered proximate mechanisms by exploring how multiple environmental factors (food and temperature) influence migration. Antagonistic effects of food restriction and increased temperature on condition and size-related traits were not translated at the level of migration tactics, where effects of food restriction and temperature were additive, but opposing (food restriction increased anadromy, whereas temperature decreased anadromy). I explored how components of metabolic rate – a fundamental determinant of physiological status – varied according to food restriction and population background in Chapter 4. Standard metabolic rate (SMR) was lower in food-deprived fish, while SMR, maximum metabolic rate, and aerobic scope (AS) were higher in offspring from a naturally anadromous population compared to a non-anadromous population. Population-specific effects of food restriction on AS also emerged. I further addressed the causes and consequences of metabolic rate variation in Chapter 5, where I found metabolic traits varied according to both population background and temperature, with important consequences for growth rates (a key fitness-related trait that can shape life histories). Collectively, these results contribute to our knowledge of how environmental and genetic factors underpin life-history diversity in terms of migratory tactics and physiology. Changes in environmental conditions will likely alter patterns of life-history diversity (mediated by changes in individual physiology) in ways that will also depend on population-specific factors. While predicting the impacts of multi-faceted environmental change will be complex, knowledge of the links between physiology, environment, and ultimately, life history, is crucial for conserving important biodiversity within brown trout, a species that is already in widespread decline due to pervasive global change.

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