Thesis (Ph.D.) - University of St Andrews, April 2006.

Historically the nutrient rich Benguela ecosystem supported large stocks of commercially important fish which sustained the Namibian fishing sector. Recently, non-exploited species i.e. bearded goby (Sufflogobius bibarbatus) and jellyfish (Chrysaora fulgida and Aequorea forskalea) have become more apparent and are described as key-species in this ecosystem. Empirical evidence for understanding the stock abundance and dynamics of S. bibarbatus and jellyfish are still sparse, as research focus has been mainly on commercially important fish. The abundance of these non-exploited species in relation to the environment and commercial species are also not well understood. Lack of methods to effectively assess jellyfish and S. bibarbatus have furthermore limited our knowledge. Acoustics can cover large water volumes and observe many trophic groups and interactions simultaneously hence currently proposed as the most reliable observation tool available to remotely study multiple species that are overlapping and widely distributed in marine ecosystems. For acoustic assessments using echo sounders, the ability to detect, identify and distinguish targets from each other and the echo ability (target strength: TS) of individual targets is pivotal to convert acoustic data from a calibrated system into significant biological measures. The lack of effective acoustic identification (ID) techniques and knowledge about TS of species may limit the application of acoustics. The swimbladder generally contributes more than 90% to the backscattered energy from fish, which makes knowledge of the swimbladder vital for understanding the acoustic properties of a fish. Prior to this study, the presence or absence of a swimbladder within S. bibarbatus has been uncertain. This thesis is an exploratory study addressing 1) the acoustic identification challenge of species in aggregating in mixed assemblages and 2) the acoustic characteristics of the target species. The latter two are of essence to assess the biomass, distributions and ecological interactions of these non-exploited. The multiple frequency data (18, 38, 70, 120 and 200 kHz) and trawl data used in this study were collected on a survey conducted by the RV G.O.Sars during April 2008 in the northern Benguela. Fifteen validated assumed to be ‘single species' trawl and acoustic datasets were selected and used in the application and developing of ID techniques. Traditional acoustic identification techniques (Sᵥ-differencing and relative frequency response r(f)) were adopted and found ineffective as standalones to discriminate the species under study. The overlaps in the Sᵥ differences of the three species complicated separation. A multivariate statistical approach, Linear Discriminant Analysis (LDA) was applied to predict which of the variables s[subscript(A)], S[subscript(A)], Δs[subscript(A)] and r(f) discriminated the three species groups from each other with a higher accuracy. It was found that by combining backscattering strength S[subscript(A)] and r(f) a correct classification accuracy of up to 95% could be obtained. Limitation is that the LDA technique as any classification method is not applicable in “real time” during surveys. A new technique, here within referred to as the Separator Technique, which incorporates the standard techniques, LDA results, a novel r(f) similarity comparison technique and a threshold s[subscript(A)] response technique was established. The effectiveness of the Separator Technique is in the recognition of similarities and stability in frequency response by simple correlation of the observed frequency response at systematic Sᵥ-threshold levels. Accurate acoustic classification depends on good and valid training datasets and there has so far not been a simple way of acoustically detecting if the selected assumed “pure” datasets is contaminated or not. Only available reliable source are the trawl samples. The r(f) similarity comparison method showed that some of the assumed ‘single species' trawls were mixed and that presence of <1% of strong scatterers could mask a weaker scatterer. By evaluating the threshold s[subscript(A)] frequency response, the proportion of thresholded backscattering could be quantified. A frequency which is more appropriate for the acoustic assessment of the respective species in mixed aggregations could also be identified. Further improvements of the Separator Technique are required in terms of the precise Sᵥ-cut levels. The presence of S. bibarbatus' swimbladder was confirmed from two thawed specimens. From further investigations on 26 dissections of sampled S. bibarbatus, the swimbladder was identified as a physoclist (closed swimbladder) with an extensive gas gland, and its morphology was roughly described as prolate spheroid shaped and with about 5ᴼ negatively tilted compared fish vertebra. This means that the strongest echo from a goby will be found when the fish is at about 5ᴼ head down relative to the horizontal. The in situ TS of 8 cm sized S. bibarbatus and the two jellyfish species: C. fulgida [umbrella diameter: 21.7 cm] and A. forskalea [16 cm] at multiple frequencies (18, 38, 70, 120 and 200 kHz) was estimated. At 38 kHz, the TS was -53 dB for S. bibarbatus, -58 dB for A. forskalea and -66 dB for C. fulgida. The single echo detection (SED) approach which is assumed to be a more accurate method for estimating TS than the previously applied methods for jellyfish. The TS results for S. bibarbatus are of similar magnitude to other published TS values of C. fulgida. This suggests that estimates of jellyfish may be overestimated due to inaccuracies in target identification. This thesis established the acoustic characteristics of jellyfish and S. bibarbatus within the northern Benguela which makes it possible to acoustically assess and monitor jellyfish and/or fish. The identification technique though still in early phases of development, can be applied to enhance quality of training datasets (samples) used in classification. This piece of work can reduce variability in biomass estimates that arises from masking or misclassification of echoes.

Medusozoan jellyfish (Classes Scyphozoa and Hydrozoa) have gained a degree of worldwide notoriety in the last fifteen years, particularly as anthropogenic influences such as climate change and overfishing push some ecosystems toward their advantage (Lynam et al. 2005, Purcell and Arai 2001, Purcell et al. 2007, Purcell 2012, Flynn et al. 2012, Dawson et al. 2014). Accordingly, both the lay and scientific media have paid a good deal of attention to jellyfish bloom phenomena and their impacts on human activities, but the bulk of this attention has been devoted to larger, visually obvious species of Class Scyphozoa. Only recently have their smaller cousins, the hydrozoans, come to be recognized as potentially problematic. This thesis examines population ecology of hydrozoan medusae (hydromedusae) and their implications for salmon aquaculture in Scotland. My review of available literature has found hydrozoans to be a recognized - though under- studied - problem for Scottish salmon (Chapter 1, Prospective monitoring of hydromedusa populations at salmon aquaculture facilities). Typically, hydrozoan populations at salmon farms have been discussed in the scientific literature only in the context of extremely dense visible blooms or in the wake of major mortality incidents. This retrospective, rather than prospective, approach has left a dearth of knowledge pertaining to hydromedusan interactions with farmed fish, with both fish welfare and industry economics vulnerable to future blooms. This thesis sought to build a basis for the goals of prediction, avoidance, and mitigation of harmful hydrozoan jellyfish blooms. First and foremost, this required the development of a prospective time-series dataset of hydromedusan occurrences at salmon farms (Chapter 2, Bacterial genera biodiversity in three medusozoan species in Shetland). To this end, four farms were recruited as participants across a three-year survey. Weekly plankton tow-based sampling at these sites identified which hydrozoan species could be expected to produce blooms, the seasonality of such blooms, and the pathological sequelae that could be expected in salmon after exposure to such blooms. Following one particularly dramatic bloom, a spike in gill pathologies in salmon was observed, followed by a spike in overall mortality and the eventual loss of up to £2.5 million value as the fish were humanely culled. This survey also demonstrated that hydromedusan blooms are usually spatially and temporally patchy, limiting the opportunities for geographically-encompassing predictive power. Instead, individual aquaculture facilities may require site-specific risk assessment and planning frameworks to monitor and cope with blooms. Potential methods for continued basic monitoring and a mitigation strategy based on minimizing contact between fish and high-density blooms are suggested. A second mitigation goal examined the theory that medusae may act as vectors for microbial pathogens, particularly Tenacibaculum maritimum (Ferguson et al. 2010, Delannoy et al. 2011; Chapter 3). Sampling methods designed to target T. maritimum were employed with the aim of determining its distribution and role as a symbiont in various life stages of medusozoan species. While T. maritimum itself was not observed, a number of other fish pathogens were found in close association with several species. This included Aeromonas salmonicida, known to cause furunculosis in aquaculture of both salmon and trout (Nomura et al. 1992). Further work is required to piece together the nature of these associations. Finally, Chapter 2 identified a particular hydrozoan genus, Obelia, as a likely significant contributor to blooms at salmon aquaculture sites. One of its species, O. geniculata, has a widely distributed and well-recognized benthic colonial life stage (called the hydroid stage) in Scottish nearshore sublittoral environments. In attempting to sample these hydroids from previously well-colonized sites in Shetland in late 2012, it became apparent that a severe local reduction in the benthic population was taking place. This allowed for the opportunity to study phylogeographic population structure - i.e. the boundaries of its gene pool(s) in Scottish waters and its potential for dispersal during one seasonal reproductive period - using a molecular study of the mitochondrial cytochrome oxidase subunit I (mtCOI) gene (Chapter 4, Phylogeographic analysis of Obelia geniculata populations in the north of Scotland). In sampling immediately after the observed dieback, O. geniculata was found to follow a south-to-north pattern of genetic grouping, as well as a confirmed dieback. However, this pattern disappeared in samples collected after the population had recovered, probably due to the immigration of genetically novel individuals. This finding, in conjunction with the spatial-temporal patchiness found in the medusa bloom stage, suggests the importance of the larval stage as the primary stage for dispersal in the plankton. This study was also able to compare present population genetic data with a set of O. geniculata mtCOI data collected between 1998 and 2002. The combined data potentially show a high degree of mixing across a number of North Atlantic regions, including Icelandic and North American sites. Further investigation will be required to discern whether this pattern is temporally based (i.e. artefact of 15 years' elapsed time in opportunities for population mixing), or whether ecological, anthropogenic, or combined mechanisms are facilitating rapid transport of propagules to yield a well-mixed population. Further work in refining prediction and mitigation is still needed, as are effective veterinary interventions in the event of blooms. Continued study into the ecological patterns of colonization and dispersal may help to minimize exposure to blooms, by helping to assess site-based risks. This research forms the basis for such studies into hydrozoan interactions with salmon farms in Scotland, and how the industry might seek to minimize their impacts.

FundaÃÃo de Amparo à Pesquisa do Estado do Cearà / As medusas sÃo importantes componentes do zooplÃncton marinho e de interesse cientÃfico devido a seus impactos ecolÃgicos, econÃmicos e de saÃde pÃblica, entretanto poucos estudos abordam a ecologia das medusas no Nordeste do Brasil. O objetivo geral da dissertaÃÃo foi: analisar a Ecologia das medusas (Cnidaria: Scyphozoa, Cubozoa) na enseada do Mucuripe em Fortaleza, Nordeste do Brasil. Os objetivos especÃficos incluem: analisar a abundÃncia; a freqÃÃncia absoluta e relativa das espÃcies de medusas e o estudo da estrutura populacional das espÃcies Lychnorhiza lucerna, Chrysaora lactea e Chiropsalmus quadrumanus. As coletas foram realizadas de janeiro de 2004 a fevereiro de 2005 atravÃs de arrasto-de-praia na enseada do Mucuripe em Fortaleza, Estado do CearÃ. A dissertaÃÃo està estruturada em 5 capÃtulos para facilitar a submissÃo a periÃdicos cientÃficos. O capÃtulo 1 aborda uma introduÃÃo geral à dissertaÃÃo com aspectos geogrÃficos, metereolÃgicos e oceanogrÃficos. O capÃtulo 2 aborda a estrutura da comunidade de medusas com anÃlise da abundÃncia e freqÃÃncia das espÃcies estudadas e estudo com tÃcnicas de agrupamento e Ãndices de diversidade, dominÃncia e eqÃitabilidade. O capÃtulo 3, 4 e 5 estudam, respectivamente, a estrutura das populaÃÃes das medusas Lychnorhiza lucerna, Chrysaora lactea e Chiropsalmus quadrumanus na enseada do Mucuripe, Nordeste do Brasil. / The jellyfishes are important components of marine zooplancton and they have scientific interest due to its impacts on the ecology, the economy and the public health, althought few studies had approached the ecology of the jellyfishes from north-eastern Brazil. The general objective of the dissertation was: to analyze the Ecology of the jellyfishes (Cnidaria: Scyphozoa, Cubozoa) in the cove of the Mucuripe in Fortaleza, Northeast of Brazil. The specific objectives include: to analyze the abundance; the absolute and relative frequency of the species of jellyfishes and the study of the population structure of the species Lychnorhiza lucerna, Chrysaora lactea and Chiropsalmus quadrumanus. The collections were done from January of 2004 to February of 2005 through trawl in the cove of the Mucuripe in Fortaleza, Cearà state. The dissertation is structured in 5 chapters to facilitate the submission for scientific journals. The chapter 1 approaches general introduction to the dissertation with meteorological, geographical and oceanographic aspects. Chapter 2 approaches the community structure of jellyfishes with the analysis of the abundance and frequency of the studied species; study with cluster, and indices of diversity, dominance and evenness. Chapters 3, 4 and 5 study, respectively, the structure of the jellyfishes populations of Lychnorhiza lucerna, Chrysaora lactea and Chiropsalmus quadrumanus in the cove of the Mucuripe, Northeast of Brazil.

As the biomass of jellyfish (medusae of the Scyphozoa and Hydrozoa) has risen in numerous locations worldwide, awareness of their potential to exert a controlling influence on marine ecosystems and hinder the recruitment of fish stocks has increased. Medusae are capable of intensive, size–selective, predation on zooplankton, which may alter the composition of the plankton community. Jellyfish are often found in dense layers, up to hundreds of metres thick, which can extend horizontally for hundreds of kilometres. Such aggregations may benefit specialist feeders, such as turtles, that rely upon jellyfish for food and those fish that are able to find refuge under the jellyfish umbrellas. Nonetheless, the predominance of jellyfish in pelagic ecosystems is not generally viewed as desirable; in fact, this situation has been portrayed as the result of pollution and overexploitation of otherwise productive seas. However, jellyfish are sensitive indicators of environmental change, and their populations appear to respond to climatic fluctuations, so jellyfish warrant study for their intrinsic ecosystem role particularly given present concerns over climate change. With growing acceptance that fishery management should take an holistic ‘ecosystem approach’, knowledge of the interactions between jellyfish, fisheries and climate may be vital in progression towards the goal of ecosystem–based sustainable management of fisheries. Unfortunately, due to their gelatinous nature, medusae are difficult to sample using conventional netting techniques and data on changes in distribution and abundance are consequently sparse. Recent studies have demonstrated that medusae can be detected acoustically and that this technique could provide a rapid and cost–effective estimate of their biomass and distribution. This thesis reports my endeavour to demonstrate the ecosystem role of medusae and to develop acoustic techniques to monitor their biomass. Through regession analyses, I link the abundance of medusae (Aurelia aurita, Cyanea lamarckii, and Cyanea capillata) in regions of the North Sea to climatic fluctuations, as quantified by the North Atlantic Oscillation Index, and show that medusae may be important indicators of regional ecosystem change. The mechanisms linking climatic fluctuations to ecosystem changes are explored via a correlative modelling approach using General Additive Models; I show that the mechanisms are location dependent and explainable in terms of direct, rapidly responding (intra–annual) influences (surface warming, river run–off, and wind–driven mixing and advection) and longer–term (interannual) oceanographic responses (changes in circulation currents i.e. the northward extent of the gulf stream and relative strength of inflow into the North Sea of the North Atlantic current, Continental Shelf Jet and Arctic waters). I present correlative evidence for a detrimental impact by Aurelia aurita on herring 0–group recruitment, once the influence of interannual change in herring spewing stock biomass on recruitment is factored out through modelling with a Ricker stock–recruitment relationship. Similarly, a commensal relationship between whiting and Cyanea spp. medusae is shown to improve North Sea whiting survival to the 1–group. In progress towards the automated acoustic identification of species, I have developed an in situ discrimination tool that can distinguish between echoes from: Aequorea aequorea; Chrysaora hysoscella; clupeid fish (sardine, anchovy and round herring); and horse mackerel/Cape hake. The technique relies upon characteristic differences in echo strength between frequencies, which are determined for each jellyfish species and finfish group using combined multifrequency acoustic and pelagic trawl samples. This method has facilitated the world’s first acoustic–based estimate of jellyfish biomass in the Namibian Benguela Sea. The 12.2 million tonnes of biomass of medusae (Aequorea aequorea and Chrysaora hysoscella) in the Namibian Benguela Sea was found to be greater than the combined biomass, 3.6 million tonnes, of commercially important fish (horse mackerel, Cape hake, sardines, anchovy, and round herring) in the same area. These results suggest that medusae may have an important role in the Benguela ecosystem that has previously been overlooked and that their biomass should be monitored.