Paul Stebbing

Horizon scanning for invasive alien species with the potential to threaten biodiversity in Great Britain

Invasive alien species (IAS) are considered one of the greatest threats to biodiversity, particularly through their interactions with other drivers of change. Horizon scanning, the systematic examination of future potential threats and opportunities, leading to prioritization of IAS threats is seen as an essential component of IAS management. Our aim was to consider IAS that were likely to impact on native biodiversity but were not yet established in the wild in Great Britain. To achieve this, we developed an approach which coupled consensus methods (which have previously been used for collaboratively identifying priorities in other contexts) with rapid risk assessment. The process involved two distinct phases: Preliminary consultation with experts within five groups (plants, terrestrial invertebrates, freshwater invertebrates, vertebrates and marine species) to derive ranked lists of potential IAS. Consensus-building across expert groups to compile and rank the entire list of potential IAS. Five hundred and ninety-one species not native to Great Britain were considered. Ninety-three of these species were agreed to constitute at least a medium risk (based on score and consensus) with respect to them arriving, establishing and posing a threat to native biodiversity. The quagga mussel, Dreissena rostriformis bugensis, received maximum scores for risk of arrival, establishment and impact; following discussions the unanimous consensus was to rank it in the top position. A further 29 species were considered to constitute a high risk and were grouped according to their ranked risk. The remaining 63 species were considered as medium risk, and included in an unranked long list. The information collated through this novel extension of the consensus method for horizon scanning provides evidence for underpinning and prioritizing management both for the species and, perhaps more importantly, their pathways of arrival. Although our study focused on Great Britain, we suggest that the methods adopted are applicable globally.

Mating behaviour and evidence for a female released courtship pheromone in the signal crayfish Pacifastacus leniusculus

The mating behaviour of the signal crayfish, Pacifastacus leniusculus (Dana), has been categorised into seven distinct stages:; orientation; contact; seizure; turning; mounting; spermatophore deposition; and dismounting. These categories were used in the development of a bioassay to test whether mature females release a sex pheromone during the breeding season to which males respond. Water conditioned by 1) mature females (MF water), 2) immature females (IF water) and 3) freshwater (C water), were injected through standard aquarium air-stones into tanks containing mature males. The behaviour of the male was recorded on video for 15 minutes before and after injection of each test water. The time that the males spent exhibiting the three behavioural categories of ‘quiescent,’ ‘motile’ and ‘handling’ of the air-stone, were recorded. ‘Handling’ of the air-stone included the mating behaviours of seizure, mounting, and spermatophore deposition onto the surface of the air-stone. Males exposed to MF water exhibited significantly increased levels of motile activity and handling behaviour, than males exposed to C water or IF water. These results demonstrate for the first time the presence of a sex pheromone, released during the breeding season by mature females, that stimulates courtship and mating behaviour in male P. leniusculus.

Biosecurity and Vector Behaviour: Evaluating the Potential Threat Posed by Anglers and Canoeists as Pathways for the Spread of Invasive Non-Native Species and Pathogens

Invasive non-native species (INNS) endanger native biodiversity and are a major economic problem. The management of pathways to prevent their introduction and establishment is a key target in the Convention on Biological Diversitys Aichi biodiversity targets for 2020. Freshwater environments are particularly susceptible to invasions as they are exposed to multiple introduction pathways, including non-native fish stocking and the release of boat ballast water. Since many freshwater INNS and aquatic pathogens can survive for several days in damp environments, there is potential for transport between water catchments on the equipment used by recreational anglers and canoeists. To quantify this biosecurity risk, we conducted an online questionnaire with 960 anglers and 599 canoeists to investigate their locations of activity, equipment used, and how frequently equipment was cleaned and/or dried after use. Anglers were also asked about their use and disposal of live bait. Our results indicate that 64% of anglers and 78.5% of canoeists use their equipment/boat in more than one catchment within a fortnight, the survival time of many of the INNS and pathogens considered in this study and that 12% of anglers and 50% of canoeists do so without either cleaning or drying their kit between uses. Furthermore, 8% of anglers and 28% of canoeists had used their equipment overseas without cleaning or drying it after each use which could facilitate both the introduction and secondary spread of INNS in the UK. Our results provide a baseline against which to evaluate the effectiveness of future biosecurity awareness campaigns, and identify groups to target with biosecurity awareness information. Our results also indicate that the biosecurity practices of these groups must improve to reduce the likelihood of inadvertently spreading INNS and pathogens through these activities.

Anisakis simplex sensu lato associated with red vent syndrome in wild adult Atlantic salmon Salmo salar in England and Wales.

Wild Atlantic salmon Salmo salar with swollen and/or bleeding vents (red vent syndrome) have been observed in rivers across England and Wales. Low numbers of salmon with this condition have previously been recorded, but reports have increased in 2006 and 2007. Affected and non-affected salmon were sampled from fish traps and their vent pathology was examined. Third stage larvae of the nematode Anisakis simplex sensu lato were observed in the tissue surrounding the vent in all affected fish. Histology of the vent showed gross lesions with an inflammatory response associated with non-encapsulated nematode worms in the connective tissue and skeletal muscle. The presence of the parasite in the unusual location of the vent areas, with associated haemorrhaging, is possibly a new emerging pathological association with the nematode A. simplex infection in Atlantic salmon. The reason for this unusual tissue tropism by larval A. simplex and the significance on already depleted salmon stocks are currently unknown.

Review of methods for the management of non-indigenous crayfish, with particular reference to Great Britain

Globally, some of the most widely distributed, damaging freshwater non-indigenous species are crayfish. With an increasing demand to meet regulatory targets, there is a need to implement more stringent controls to prevent further environmental stress and irreparable shifts in species diversity attributed to non-indigenous crayfish. In establishing a management strategy for non-indigenous crayfish in Great Britain (GB), consideration needs to be given to: (1) the prevention of further introductions of species, including novel species and those already established; (2) methods for containing and preventing the further spread of established populations, and (3) methods for eradication/control. This review aims to provide a critique of existing and potential management methods (mechanical, physical, biological, biocidal, autocidal, legislative) and how they can be potentially used in a cohesive, intergrated and comprehensive strategy with particular reference to GB and the management of the signal crayfish Pacifastacus leniusculus.

Developing a framework of minimum standards for the risk assessment of alien species

1. Biological invasions are a threat to biodiversity, society and the economy. There is an urgent need to provide evidence-based assessments of the risks posed by inva-sive alien species (IAS) to prioritize action. Risk assessments underpin IAS policies in many ways: informing legislation; providing justification of restrictions in trade or consumer activities; prioritizing surveillance and rapid response. There are benefits to ensuring consistency in content of IAS risk assessments globally, and this can be achieved by providing a framework of minimum standards as a checklist for quality assurance. 2. From a review of existing risk assessment protocols, and with reference to the r equirements of the EU Regulation on IAS (1143/2014) and international agreements including the World Trade Organisation, Convention on Biological Diversity and International Plant Protection Convention, coupled with consensus methods, we identified and agreed upon 14 minimum standards (attributes) a risk-assessment scheme should include. 3. The agreed minimum standards were as follows: (1) basic species description; (2) likelihood of invasion; (3) distribution, spread and impacts; (4) assessment of intro-duction pathways; (5) assessment of impacts on biodiversity and ecosystems; (6) Assessment of impact on ecosystem services; (7) assessment of socio-economic impacts; (8) consideration of status (threatened or protected) of species or habitat under threat; (9) assessment of effects of future climate change; (10) completion possible even when there is a lack of information; (11) documents information sources; (12) provides a summary in a consistent and interpretable form; (13) includes uncertainty; (14) includes quality assurance. In deriving these minimum standards, gaps in knowledge required for completing risk assessments and the scope of exist-ing risk assessment protocols were revealed, most notably in relation to assessing benefits, socio-economic impacts and impacts on ecosystem services but also inclu-sion of consideration of climate change. 4. Policy implications. We provide a checklist of components that should be within in-vasive alien species risk assessments and recommendations to develop risk assess-ments to meet these proposed minimum standards. Although inspired by implementation of the European Union Regulation on invasive alien species, and as such developed specifically within a European context, the derived framework and minimum standards could be applied globally.

Predicting and mapping the risk of introduction of marine non-indigenous species into Great Britain and Ireland

Non-indigenous species (NIS) can have adverse environmental, economic and social impacts. Their management is now incorporated into key legislation, including the European Union (EU) Marine Strategy Framework Directive and the EU Regulation on the prevention and management of the introduction and spread of invasive alien species. Prevention of NIS introductions and the early detection of NIS following their introduction are recognised as the most effective approaches for reducing the potential impacts of NIS. This is true for most aquatic environments but especially so for the marine environment, where control and/or eradication are often not achievable. By assessing introduction vector activity, it is possible to identify coastal areas and specific locations where marine NIS may be more likely to be introduced. This study uses data relating to the activity of key introduction vectors; shipping, recreational boating and live animal aquaculture import, to estimate the relative risk of introduction of NIS around coastal regions of Great Britain and Ireland. Spatial analysis was used to create “heat” maps indicating coastal areas of increased relative risk of introduction of NIS by these vectors. The results of the present study will be crucial for the implementation of targeted vector management plans, supporting preventive strategies, and will facilitate a risk analyses of NIS threats to inform monitoring and surveillance programmes.

Parahepatospora carcini n. gen., n. sp., a parasite of invasive Carcinus maenas with intermediate features of sporogony between the Enterocytozoon clade and other microsporidia

Parahepatospora carcini n. gen. n. sp., is a novel microsporidian parasite discovered infecting the cytoplasm of epithelial cells of the hepatopancreas of a single Carcinus maenas specimen. The crab was sampled from within its invasive range in Atlantic Canada (Nova Scotia). Histopathology and transmission electron microscopy were used to show the development of the parasite within a simple interfacial membrane, culminating in the formation of unikaryotic spores with 5-6 turns of an isofilar polar filament. Formation of a multinucleate meront (>12 nuclei observed) preceded thickening and invagination of the plasmodial membrane, and in many cases, formation of spore extrusion precursors (polar filaments, anchoring disk) prior to complete separation of pre-sporoblasts from the sporogonial plasmodium. This developmental feature is intermediate between the Enterocytozoonidae (formation of spore extrusion precursors within the sporont plasmodium) and all other Microsporidia (formation of spore extrusion precursors after separation of sporont from the sporont plasmodium). SSU rRNA-based gene phylogenies place P. carcini within microsporidian Clade IV, between the Enterocytozoonidae and the so-called Enterocytospora-clade, which includes Enterocytospora artemiae and Globulispora mitoportans. Both of these groups contain gut-infecting microsporidians of aquatic invertebrates, fish and humans. According to morphological and phylogenetic characters, we propose that P. carcini occupies a basal position to the Enterocytozoonidae. We discuss the discovery of this parasite from a taxonomic perspective and consider its origins and presence within a high profile invasive host on the Atlantic Canadian coastline.

The response to disturbance chemicals and predator odours of juvenile and adult signal crayfish Pacifastacus leniusculus (Dana)

Many species of crayfish have been shown to use disturbance chemicals to detect the presence of predators and other dangers, yet there have been no investigations in adults or juveniles of Pacifastacus leniusculus, a key species, particularly for invasive species study. Juveniles and adults were exposed to conditioned water from stressed and damaged conspecific males. Both responded to these odours, but did not respond to water from stressed or damaged males with blocked nephropores. Urine from stressed and damaged males also elicited a significant response, which was much stronger than that of conditioned water. Odours from urine and water of damaged individuals induced a greater response than stress odours. We propose that chemicals released by stressed or damaged Pa. leniusculus are the same substance, but quantities released in the urine vary in context-specific circumstances. Predator-odour conditioned water from Perca fluviatilis elicited no response, but conditioned Anguilla anguilla water stimulated significant responses in juveniles and adults. Juveniles exhibited the strongest responses to all odours. These results show that Pa. leniusculus utilises both conspecific and heterospecific sources of info-chemicals to assess risk in the environment, which may contribute to its success as an invasive species and give it a competitive advantage.

Parasites, pathogens and commensals in the “low-impact” non-native amphipod host Gammarus roeselii

BackgroundWhilst vastly understudied, pathogens of non-native species (NNS) are increasingly recognised as important threats to native wildlife. This study builds upon recent recommendations for improved screening for pathogens in NNS by focusing on populations of Gammarus roeselii in Chojna, north-western Poland. At this location, and in other parts of continental Europe, G. roeselii is considered a well-established and relatively ‘low-impact’ invader, with little understanding about its underlying pathogen profile and even less on potential spill-over of these pathogens to native species.ResultsUsing a combination of histological, ultrastructural and phylogenetic approaches, we define a pathogen profile for non-native populations of G. roeselii in Poland. This profile comprised acanthocephalans (Polymorphus minutus Goese, 1782 and Pomphorhynchus sp.), digenean trematodes, commensal rotifers, commensal and parasitic ciliated protists, gregarines, microsporidia, a putative rickettsia-like organism, filamentous bacteria and two viral pathogens, the majority of which are previously unknown to science. To demonstrate potential for such pathogenic risks to be characterised from a taxonomic perspective, one of the pathogens, a novel microsporidian, is described based upon its pathology, developmental cycle and SSU rRNA gene phylogeny. The novel microsporidian Cucumispora roeselii n. sp. displayed closest morphological and phylogenetic similarity to two previously described taxa, Cucumispora dikerogammari (Ovcharenko & Kurandina, 1987), and Cucumispora ornata Bojko, Dunn, Stebbing, Ross, Kerr & Stentiford, 2015.ConclusionsIn addition to our discovery extending the host range for the genus Cucumispora Ovcharenko, Bacela, Wilkinson, Ironside, Rigaud & Wattier, 2010 outside of the amphipod host genus Dikerogammarus Stebbing, we reveal significant potential for the co-transfer of (previously unknown) pathogens alongside this host when invading novel locations. This study highlights the importance of pre-invasion screening of low-impact NNS and, provides a means to document and potentially mitigate the additional risks posed by previously unknown pathogens.