Shining a light on parasite behaviour: daily patterns of Argulus fish lice

Parasites display a wide range of behaviours that are frequently overlooked in favour of host responses. Understanding these behaviours can improve parasite control through a more precise application or development of new behaviour-based strategies. In aquaculture fish lice are an ongoing problem, infections reduce fishery production and control options are limited. Fish lice are distinct in their ability to survive and swim off hosts, allowing the transmission to multiple fish hosts across their lifespan. Here we assessed the off-host behaviour of Argulus foliaceus (a freshwater fish louse) and observed a diurnal rhythmical pattern in their behaviour. This pattern was lost when lice were exposed to constant darkness, indicating that the behaviour is not endogenously driven. Males were consistently active in light with reduced activity in darkness. In contrast, females were active during light and dark phases with peak activity at the start of dark periods. A. foliaceus was also strongly attracted to a light stimulus, preferring white- and blue-coloured lights over green- or red-coloured lights. Light is a strong driver of fish louse activity and could be used to trap parasites. Aquaculture light regimes could also be altered to reduce parasite attraction and activity

Saprolegnia parasitica zoospore activity and host survival indicates isolate variation in host preference

The ubiquitous freshwater pathogen Saprolegnia parasitica has long been considered a true generalist, capable of infecting a wide range of fish species. It remains unclear, however, whether different isolates of this pathogen, obtained from distinct geographic locations and host species, display differences in host preference. To assess this, the current study examined the induced zoospore encystment responses of four S. parasitica isolates towards the skin of four fish species. While three of the isolates displayed ‘specialist’ responses, one appeared to be more of a ‘generalist’. In vivo challenge infections involving salmon and sea trout with the ‘generalist’ (salmon isolate EA001) and a ‘specialist’ (sea trout isolate EA016) pathogen, however, did not support the in vitro findings, with no apparent host preference reflected in infection outcomes. Survival of sea trout and salmon though was significantly different following a challenge infection with the sea trout (EA016) isolate. These results indicate that while S. parasitica isolates can be considered true generalists, they may target hosts to which they have been more frequently exposed (potential local adaptation). Understanding host preference of this pathogen could aid our understanding of infection epidemics and help with the development of fish management procedures

Circadian dynamics of the teleost skin immune-microbiome interface

Background Circadian rhythms of host immune activity and their microbiomes are likely pivotal to health and disease resistance. The integration of chronotherapeutic approaches to disease mitigation in managed animals, however, is yet to be realised. In aquaculture, light manipulation is commonly used to enhance growth and control reproduction but may have unknown negative consequences for animal health. Infectious diseases are a major barrier to sustainable aquaculture and understanding the circadian dynamics of fish immunity and crosstalk with the microbiome is urgently needed. Results Here, using rainbow trout (Oncorhynchus mykiss) as a model, we combine 16S rRNA metabarcoding, metagenomic sequencing and direct mRNA quantification methods to simultaneously characterise the circadian dynamics of skin clock and immune gene expression, and daily changes of skin microbiota. We demonstrate daily rhythms in fish skin immune expression and microbiomes, which are modulated by photoperiod and parasitic lice infection. We identify putative associations of host clock and immune gene profiles with microbial composition. Our results suggest circadian perturbation, that shifts the magnitude and timing of immune and microbiota activity, is detrimental to fish health. Conclusions The substantial circadian dynamics and fish host expression-microbiome relationships we find represent a valuable foundation for investigating the utility of chronotherapies in aquaculture, and more broadly contributes to our understanding of the role of microbiomes in circadian health of vertebrates

Evidence for cryptic speciation in directly transmitted Gyrodactylid parasites of Trinidadian guppies

Cryptic species complexes are common among parasites, which tend to have large populations and are subject to rapid evolution. Such complexes may arise through host-parasite co-evolution and/or host switching. For parasites that reproduce directly on their host, there might be increased opportunities for sympatric speciation, either by exploiting different hosts or different micro-habitats within the same host. The genus Gyrodactylus is a specious group of viviparous monogeneans. These ectoparasites transfer between teleosts during social contact and cause significant host mortality. Their impact on the guppy (Poecilia reticulata), an iconic evolutionary and ecological model species, is well established and yet the population genetics and phylogenetics of these parasites remains understudied. Using mtDNA sequencing of the host and its parasites, we provide evidence of cryptic speciation in Gyrodactylus bullatarudis, G. poeciliae and G. turnbulli. For the COII gene, genetic divergence of lineages within each parasite species ranged between 5.7 and 17.2%, which is typical of the divergence observed between described species in this genus. Different lineages of G. turnbulli and G. poeciliae appear geographically isolated, which could imply allopatric speciation. In addition, for G. poeciliae, co-evolution with a different host species cannot be discarded due to its host range. This parasite was originally described on P. caucana, but for the first time here it is also recorded on the guppy. The two cryptic lineages of G. bullatarudis showed considerable geographic overlap. G. bullatarudis has a known wide host range and it can also utilize a killifish (Anablepsoides hartii) as a temporary host. This killifish is capable of migrating overland and it could act as a transmission vector between otherwise isolated populations. Additional genetic markers are needed to confirm the presence of these cryptic Gyrodactylus species complexes, potentially leading to more in-depth genetic, ecological and evolutionary analyses on this multi-host-parasite system

Moving towards improved surveillance and earlier diagnosis of aquatic pathogens: from traditional methods to emerging technologies

Early and accurate diagnosis is key to mitigating the impact of infectious diseases, along with efficient surveillance. This however is particularly challenging in aquatic environments due to hidden biodiversity and physical constraints. Traditional diagnostics, such as visual diagnosis and histopathology, are still widely used, but increasingly technological advances such as portable next generation sequencing (NGS) and artificial intelligence (AI) are being tested for early diagnosis. The most straightforward methodologies, based on visual diagnosis, rely on specialist knowledge and experience but provide a foundation for surveillance. Future computational remote sensing methods, such as AI image diagnosis and drone surveillance, will ultimately reduce labour costs whilst not compromising on sensitivity, but they require capital and infrastructural investment. Molecular techniques have advanced rapidly in the last 30 years, from standard PCR through loop‐mediated isothermal amplification (LAMP) to NGS approaches, providing a range of technologies that support the currently popular eDNA diagnosis. There is now vast potential for transformative change driven by developments in human diagnostics. Here we compare current surveillance and diagnostic technologies with those that could be used or developed for use in the aquatic environment, against three gold standard ideals of high sensitivity, specificity, rapid diagnosis, and cost‐effectiveness

Fish swimming kinematics in a turbulent wake: to spill or not to spill?

Due to the complex nature of fish-environment interactions, the effects of altered flow conditions on fish habitats and behaviour, particularly near obstructions, are not yet fully understood. Many hydro-engineering structures generate three-dimensional turbulent structures that differ in properties from naturally occurring ones, and are challenging to fish movement. Here, swimming stability and habitat usage of Nile tilapia (Oreochromis niloticus) were examined in the turbulent wake of a horizontally oriented cylinder (50 mm diameter, D) for a series of increasing cylinder Reynolds numbers (Red). Velocity statistics showed that the near wake downstream of the cylinder within a 2D distance had higher magnitudes of longitudinal, vertical and lateral velocity components as well as Reynolds stresses, turbulence intensity and turbulent kinetic energy than the remaining wake flow field. Flow accelerating over the cylinder top and underside generated two shear horizontal layers, where two coherent structures were formed due to the shear layer breakdown off the cylinder’s walls and alternating von Karman-type vortex shedding occurred in the wake of the cylinder. The eddy symmetry and vorticity off the cylinder’s edges was dependent on Red. The recorded total number of spills, defined as loss of balance, was inversely proportional to fish length and weight, and depended on proximity to the cylinder and the flume bed. Furthermore, the frequency of spills was closely linked to the orientation of vortices and magnitude of Reynolds stresses, suggesting that these parameters may govern the swimming stability of fishes. This information may be used to inform the design of fish-friendly obstacles including hydraulic structures and hydro turbines in riverine and estuarine systems

Invisible plastics problem in intensive aquaculture: The case of polyvinylpyrrolidone

For over 70 years, aquaculture practices have relied on the same methods for biosecurity, however epidemics remain a primary limitation of global aquaculture yields with billions in revenue being lost every year due to disease. The intense nature of fish and shellfish farming necessitates the regular use of synthetic chemicals as both preventive and treatment measures, covering broodstocks to hatching and continuing through all stages of rearing. This practice, however, results in the contamination of rearing environments with persistent xenobiotics. A specific drawback in this foundational strategy for aquaculture biosecurity is highlighted in the current review: the consistent use of a water‐soluble polymer polyvinylpyrrolidone (PVP) across most, if not all, stages of rearing aquacultural livestock. PVP is used intensively within aquaculture practices as it is a ubiquitous additive within commercially available germicidal, prophylactic, and therapeutic products applied to control and prevent disease outbreaks within aquacultural farms. As a polymer, PVP is synthetic and biodegradation‐resistant, and has recently been described as an emerging contaminant of freshwater ecosystems. It is well documented that other persistent, synthetic polymer pollutants such as microplastics, reduce the fecundity, growth, and significantly deplete immune function in commercially important aquatic species. Despite this, intentionally added persistent soluble polymers, such as PVP, have not been considered in the context of aquaculture productivity. This review explores the potential impact of PVP on fish and shellfish highlighting the need for aquaculture to adopt sustainable chemical practices, drawing inspiration from advancements in nanotechnology applied within human medicines to address biosecurity protocol deficiencies

To clean or not to clean: cleaning mutualism breakdown in a tidal environment

The dynamics and prevalence of mutualistic interactions, which are responsible for the maintenance and structuring of all ecological communities, are vulnerable to changes in abiotic and biotic environmental conditions. Mutualistic outcomes can quickly shift from cooperation to conflict, but it unclear how resilient and stable mutualistic outcomes are to more variable conditions. Tidally controlled coral atoll lagoons that experience extreme diurnal environmental shifts thus provide a model from which to test plasticity in mutualistic behavior of dedicated (formerly obligate) cleaner fish, which acquire all their food resources through client interactions. Here, we investigated cleaning patterns of a model cleaner fish species, the bluestreak wrasse (Labroides dimidiatus), in an isolated tidal lagoon on the Great Barrier Reef. Under tidally restricted conditions, uniquely both adults and juveniles were part‐time facultative cleaners, pecking on Isopora palifera coral. The mutualism was not completely abandoned, with adults also wandering across the reef in search of clients, rather than waiting at fixed site cleaning stations, a behavior not yet observed at any other reef. Contrary to well‐established patterns for this cleaner, juveniles appeared to exploit the system, by biting (“cheating”) their clients more frequently than adults. We show for the first time, that within this variable tidal environment, where mutualistic cleaning might not represent a stable food source, the prevalence and dynamics of this mutualism may be breaking down (through increased cheating and partial abandonment). Environmental variability could thus reduce the pervasiveness of mutualisms within our ecosystems, ultimately reducing the stability of the system