Diseased fish in the freshwater trade: from retailers to private aquarists

Millions of fish are transported between countries annually for the aquarium trade, yet no quantitative study has examined how disease frequency differs among species and stakeholders. Here we visually inspected freshwater fish species in 12 specialised and non-specialised aquarium retailers in Spain for the presence of diseased fish in 2015 and in 2016. This information was complemented with disease records from 3 internet fora (>100 000 users) and pathogen identification at a retailer. Overall, 22 fish species out of the 312 recorded were reported diseased, with species of Poeciliidae accounting for most records. Ichthyophthirius, dropsy, bacterial and monogenean infections were the most common diseases, but disease frequency differed amongst retailers and private aquarists. Although only 11 fish species at retailers were deemed unhealthy, they were popular species amongst aquarists. We encourage improved management of fish stocks, and more education campaigns to promote fish welfare and avoid misdiagnosis in the Spanish aquarium hobby

The selective cleaning behaviour of juvenile blue-headed wrasse (Thalassoma bifasciatum) in the Caribbean

Through the removal of parasites, dead skin and mucus from the bodies of visiting reef fish (clients), cleaner fish have a significant ecosystem function in the ecology of coral reefs. Cleaners gain nutrition from these interactions and through offering a ‘service’ are afforded protection from predators. Given these benefits, it is unclear why more fish do not engage in cleaning, and why part-time cleaning strategies exist. On coral reefs, dedicated species clean throughout their life, whereas some species are facultative, employing opportunistic and/or temporary cleaning strategies. Here, we investigate the cleaning behaviour of a facultative species to assess the relative importance of this interaction to the cleaner. Using a combination of focal and event sampling from a coral reef in Tobago, we show that cleaning is not an essential food source for facultative juvenile blue-headed wrasse (Thalassoma bifasciatum), as cleaning rate was unrelated to their foraging rate on the substrate. These wrasse displayed two cleaning strategies: stationary versus wandering cleaning, with cleaning frequency being highest for stationary cleaners. A specific cleaning location facilitated increased cleaning frequency, and wrasse cleaning rate decreased as cleaner or client abundance increased. We also compared juvenile blue-headed wrasse cleaning behaviour to a resident dedicated cleaner, the sharknose goby (Elacatinus evelynae), and showed that, in comparison, juvenile wrasse clean a narrower client range, predominately cleaning three species of gregarious free-ranging surgeonfish (Acanthurus spp.). The wrasse, however, frequently approached these clients without cleaning, which suggests that their selective cleaning strategy may be driven by the acquisition of a particular parasitic food source. Juvenile blue-headed wrasse are generalist foragers, and may thus be limited in their cleaning behaviour by their nutritional requirements, the availability of a suitable cleaning site, and fish density, which ultimately means that they do not adopt more dedicated cleaning roles within the reef community

Parasite-mediated host behavioural modifications: Gyrodactylus turnbulli infected Trinidadian guppies increase contact rates with uninfected conspecifics

While group formation provides antipredatory defences, increases foraging efficiency and mating opportunities, it can be counterintuitive by promoting disease transmission amongst social hosts. Upon introduction of a pathogen, uninfected individuals often modify their social preferences to reduce infection risk. Infected hosts also exhibit behavioural changes, for example, removing themselves from a group to prevent an epidemic. Conversely, here we show how Trinidadian guppies infected with a directly transmitted ectoparasite, Gyrodactylus turnbulli, significantly increase their contact rates with uninfected conspecifics. As uninfected fish never perform this behaviour, this is suggestive of a parasite-mediated behavioural response of infected hosts, presumably to offload their parasites. In the early stages of infection, however, such behavioural modifications are ineffective in alleviating parasite burdens. Additionally, we show that fish exposed to G. turnbulli infections for a second time, spent less time associating than those exposed to parasites for the first time. We speculate that individuals build and retain an infection cue repertoire, enabling them to rapidly recognize and avoid infectious conspecifics. This study highlights the importance of considering host behavioural modifications when investigating disease transmission dynamics

Chronic nitrate enrichment decreases severity and induces protection against an infectious disease

Excessive fertilisation is one of the most pernicious forms of global change resulting in eutrophication. It has major implications for disease control and the conservation of biodiversity. Yet, the direct link between nutrient enrichment and disease remains largely unexplored. Here, we present the first experimental evidence that chronic nitrate enrichment decreases severity and induces protection against an infectious disease. Specifically, this study shows that nitrate concentrations ranging between 50 and 250 mg NO3−/l reduce Gyrodactylus turnbulli infection intensity in two populations of Trinidadian guppies Poecilia reticulata, and that the highest nitrate concentration can even clean the parasites from the fish. This added to the fact that host nitrate pre-exposure altered the fish epidermal structure and reduced parasite intensity, suggests that nitrate protected the host against the disease. Nitrate treatments also caused fish mortality. As we used ecologically-relevant nitrate concentrations, and guppies are top-consumers widely used for mosquito bio-control in tropical and often nutrient-enriched waters, our results can have major ecological and social implications. In conclusion, this study advocates reducing nitrate level including the legislative threshold to protect the aquatic biota, even though this may control an ectoparasitic disease

Fish responses to flow velocity and turbulence in relation to size, sex and parasite load

Riverine fish are subjected to heterogeneous flow velocities and turbulence and may use this to their advantage by selecting regions that balance energy expenditure for station holding while maximizing energy gain through feeding opportunities. This study investigated microhabitat selection by guppies Poecilia reticulata in terms of flow characteristics generated by hemisphere boulders in an open channel flume. Velocity and turbulence influenced the variation in swimming behaviour with respect to size, sex and parasite intensity. With increasing body length, fish swam further and more frequently between boulder regions. Larger guppies spent more time in the areas of high-velocity and low-turbulence regions beside the boulders, whereas smaller guppies frequented the low-velocity and high-turbulence regions directly behind the boulders. Male guppies selected the regions of low velocity, indicating possible reduced swimming ability owing to hydrodynamic drag imposed by their fins. With increasing Gyrodactylus turnbulli burden, fish spent more time in regions with moderate velocity and lowest turbulent kinetic energy which were the most spatially and temporally homogeneous in terms of velocity and turbulence. These findings highlight the importance of heterogeneous flow conditions in river channel design owing to the behavioural variability within a species in response to velocity and turbulence

Assessing the invasion potential of non-native branchiobdellidans: experimental studies of survival, reproduction and competition

The impact of invasive species on the recipient ecosystem can be strongly influenced by the presence of associated symbionts. It is therefore important to evaluate the likelihood of co-introduced symbiont establishment, and this requires an understanding of their life history traits. Here, we investigate survival, reproduction and competition in two non-native branchiobdellidan ectosymbionts (Xironogiton victoriensis and Cambarincola aff. okadai) on invasive signal crayfish (Pacifastacus leniusculus). In vivo, X. victoriensis established viable infrapopulations within 10 weeks, whereas C. aff. okadai went extinct within 2 weeks. Both X. victoriensis and C. aff. okadai deposited cocoons in vivo that hatched in 10–27 and 10–11 days, respectively. In vitro, X. victoriensis and C. aff. okadai survived for over 13 and 15 weeks respectively, although both were negatively affected by increased temperature and nitrate, and were absent from kick samples taken in the field. Only C. aff. okadai deposited cocoons in vitro, and this larger species readily predated on X. victoriensis but not vice versa. Both branchiobdellidans possess traits associated with colonisation success, including a relatively fast reproductive rate and extended off-host survival. Given its survival in vivo and known detrimental effect on signal crayfish X. victoriensis is perhaps more likely to influence host invasion dynamics, although its persistence may be affected by the presence of co-occurring symbionts

The description of Gyrodactylus corleonis sp. n. and G. neretum sp. n. (Platyhelminthes: Monogenea) with comments on other gyrodactylids parasitizing pipefish (Pisces: Syngnathidae)

The current work describes two new species of Gyrodactylus von Nordmann, 1832 collected from pipefish Syngnathus scovelli (Evermann et Kendall) and Syngnathus typhle L. during two separate gyrodactylosis episodes on fish held in a public aquarium located in northern Italy. The gyrodactylids collected from the skin, fins and gills of pipefish were subjected to a morphological analysis of the attachment hooks and the morphometric data were compared to the four species of Gyrodactylus previously described from syngnathid hosts, namely G. eyipayipi Vaughan, Christison, Hansen et Shinn, 2010, G. pisculentus Williams, Kritsky, Dunnigan, Lash et Klein, 2008, G. shorti Holliman, 1963 and G. syngnathi Appleby, 1996. Principal components analysis (PCA) of the morphological data indicated six clusters; two discrete groups among the specimens taken from the pipefish held in the Italian aquarium and four further groups representing G. eyipayipi, G. pisculentus, G. shorti and G. syngnathi. Molecular sequences of the ribosomal internal transcribed spacers (ITS1 and ITS2) and the 5.8S gene for the new species considered here were then compared with those available for other species in GenBank. The comparison did not reveal any identical match, supporting the morphological analysis that Gyrodactylus corleonis sp. n. from S. typhle and Gyrodactylus neretum sp. n. from S. scovelli represent distinct species. Both G. corleonis and G. neretum possess robust hamuli, marginal hook blades that curve smoothly from their sickle base to a point beyond the toe and, ventral bars with a broad median portion and a reduced membrane. Gyrodactylus corleonis, however, can be distinguished on the basis of its heart-shaped ventral bar; G. neretum has a 1:2 hamulus point:shaft ratio and a rectangular-shaped ventral bar. A redescription of the haptoral hard parts of the four species previously recorded on pipefish is also presented

Apparent interspecific transmission of Aphanomyces astaci from invasive signal to virile crayfish in a sympatric wild population

The crayfish plague pathogen (Aphanomyces astaci) causes mass mortalities of European crayfish when transmitted from its original North American crayfish hosts. Little is known, however, about interspecific transmission of the pathogen between different American crayfish species, although evidence from trade of ornamental crayfish suggests this may happen in captivity. We screened signal and virile crayfish for A. astaci at allopatric and sympatric sites in a UK river. Whilst the pathogen was detected in signal crayfish from both sites, infected virile crayfish were only found in sympatry. Genotyping of A. astaci from virile crayfish suggested the presence of a strain related to one infecting British signal crayfish. We conclude that virile crayfish likely contracted A. astaci interspecifically from infected signal crayfish. Interspecific transmission of A. astaci strains differing in virulence between American carrier species may influence the spread of this pathogen in open waters with potential exacerbated effects on native European crayfish

Experimental investigation of physical leaky barrier design implications on juvenile rainbow trout ( Oncorhynchus mykiss ) movement

Rivers have been subject to the construction of numerous small-scale anthropogenic structures, causing alteration and fragmentation of habitats. Despite their impact on fish habitat selection, migration and swimming performance, more hydraulic structures are being added to riverine systems. These mainly have the purpose of harnessing renewable energy or mitigating the impact of flooding, as in the case of leaky barriers that are widely used for natural flood management. By providing a sustainable and cost-effective supplement to traditional hard engineering flood risk management methods, these channel-spanning wooden barriers are constructed using sustainable, local materials, intended to slow down surface water and groundwater flow, reduce flood peaks, and attenuate the flow reaching downstream communities. Despite their increasing popularity, little is known about the design implications on fish movement or hydrodynamics. Using scaled laboratory flume experiments we investigate how the physical design of four leaky barriers varying in porosity, length, provision of overhead cover, and color, impacts on fish movement and spatial usage, and the channel hydrodynamics. Our fish behavioral analysis reveals that juvenile rainbow trout (Oncorhynchus mykiss) movement reduces with barrier presence. Upstream passage increases with barrier color but not cover, for shorter rather than longer leaky barriers, and for a non-porous barrier compared to its porous counterpart. Barrier specific flow alterations appear to play a secondary role compared to barrier color. Our study showed that physical barrier design and leaky barrier presence alter fish movement, and therefore care needs to be taken during the design of such natural flood management structures

Spatial and temporal parasite dynamics: microhabitat preferences and infection progression of two co-infecting gyrodactylids

Background Mathematical modelling of host-parasite systems has seen tremendous developments and broad applications in theoretical and applied ecology. The current study focuses on the infection dynamics of a gyrodactylid-fish system. Previous experimental studies have explored the infrapopulation dynamics of co-infecting ectoparasites, Gyrodactylus turnbulli and G. bullatarudis, on their fish host, Poecilia reticulata, but questions remain about parasite microhabitat preferences, host survival and parasite virulence over time. Here, we use more advanced statistics and a sophisticated mathematical model to investigate these questions based on empirical data to add to our understanding of this gyrodactylid-fish system. Methods A rank-based multivariate Kruskal-Wallis test coupled with its post-hoc tests and graphical summaries were used to investigate the spatial and temporal parasite distribution of different gyrodactylid strains across different host populations. By adapting a multi-state Markov model that extends the standard survival models, we improved previous estimates of survival probabilities. Finally, we quantified parasite virulence of three different strains as a function of host mortality and recovery across different fish stocks and sexes. Results We confirmed that the captive-bred G. turnbulli and wild G. bullatarudis strains preferred the caudal and rostral regions respectively across different fish stocks; however, the wild G. turnbulli strain changed microhabitat preference over time, indicating microhabitat preference of gyrodactylids is host and time dependent. The average time of host infection before recovery or death was between 6 and 14 days. For this gyrodactylid-fish system, a longer period of host infection led to a higher chance of host recovery. Parasite-related mortalities are host, sex and time dependent, whereas fish size is confirmed to be the key determinant of host recovery. Conclusion From existing empirical data, we provided new insights into the gyrodactylid-fish system. This study could inform the modelling of other host-parasite interactions where the entire infection history of the host is of interest by adapting multi-state Markov models. Such models are under-utilised in parasitological studies and could be expanded to estimate relevant epidemiological traits concerning parasite virulence and host survival