Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish

The trade of live ornamental freshwater crayfish has grown rapidly in the last decade and has become the major pathway for new non-indigenous crayfish species (NICS) introductions into Europe. Here, I report on the German ornamental crayfish trade, the main importer of non-indigenous crayfish into Europe. In total, 120 NICS have been available as ornamental aquarium species. One hundred and five species originate from North or Central America and are, therefore, suspected to be crayfish plague vectors. The import rate since 2005 was estimated to be seven new species per year. Despite many species being imported, only eleven species were found to be very common in the trade. In 2009, 16 online shops offered at least 37 NICS. The availability, price, and size of the offered species were used to predict their introduction status. Multiple binary logistic regression analysis showed that species?? availability and size were the principal predictors of the likelihood of being recorded as introduced from aquaria. NICS introduced from aquaria were found to be more available and larger than those present only in aquaria, and their potential invasiveness was also higher. The findings are consistent with the propagule pressure hypothesis in that a greater availability is likely related to more release events, and large species may be released more frequently as a result of overpopulating or outgrowing their aquaria. Efforts to mitigate the risk of further harmful crayfish introductions from aquaria should aim to drastically reduce the availability of high-risk species.     

The bad and the super-bad: prioritising the threat of six invasive alien to three imperilled native crayfishes

Multiple species invasions and limited resources for management require prioritisation of deleterious effects of invaders on imperilled native species. This study prioritises the threat of six non-indigenous crayfish species (NICS) to three indigenous crayfish species (ICS) in southwestern Germany, a European region with high diversity of crayfish species and freshwater habitats. Using multivariate statistical analyses and niche-based species distribution models, the (1) contemporary and potential range overlap, (2) habitat overlap, and (3) rate of spread of the nine species were assessed. Predicted and contemporary range overlap with ICS was consistently the highest for the alien signal crayfish. Environmental niches of ICS tended to be associated with cooler temperatures (except for white-clawed crayfish), lower Human Influence Index, and higher terrain slope than that of alien Orconectes and Procambarus species, but were mostly similar to that of signal crayfish. Habitat overlap was found to be the highest between signal crayfish and ICS. In contrast to Orconectes and Procambarus species, signal crayfish also invade headwaters, where the most ICS populations occur. Range expansion during the past 15 years was the highest for signal crayfish, followed by Orconectes species. Because of the great potential to invade as-yet isolated refuge areas and spread at a high rate, signal crayfish is of the highest concern for conservation of ICS and should be primarily targeted by prevention and control measures. However, it merely represents the ‘worst of the worst’, since all NICS of North American origin are natural reservoirs of crayfish plague, a fatal disease of ICS.     

Threat of non-native crayfish introductions into Turkey: global lessons

Introductions of crayfish species from their home range to new environments have been carried out in many parts of the world. The most important introduced crayfish species are Procambarus clarkii, Pacifastacus leniusculus, Cherax destructor, C. quadricarinatus, Orconectes limosus, O. rusticus and Astacus leptodactylus. The environmental impact of crayfish introductions can be positive, negative or neutral. However, native crayfish populations in Europe have been negatively affected by introductions of non-indigenous crayfish species from America. Negative effects of non-native crayfish introductions included displacement of native crayfish species, transfer of disease (crayfish plague), consumption of fish eggs, reduction of fish stocks, consumption of large amounts of macrophytes, indirect and direct effects on other invertebrates and upsetting production in rice fields. As a result of non-native crayfish introductions, the natural harvest and crayfish industry in Europe have been severely affected. Large quantities of Turkish A. leptodactylus were harvested (approximately 7,000 tonnes annually) and exported to Europe before the crayfish plague was observed in these populations. The total harvest of A. leptodactylus in Turkey reduced dramatically to 320 in 1991 after the plague. Therefore, although Turkey currently has no known non-native crayfish species, there is a threat of non-native crayfish introduction in order to increase crayfish productions and subsequent harvest. The North American spiny-cheek crayfish, O. limosus, has been spreading quickly down the River Danube and could soon reach neighboring countries including Turkey. The North American signal crayfish, P. leniusculus is known from Greece and could be a threat to native stocks if it is introduced into Turkey for aquaculture. Additional threats may come from the release of other North American species, which are widely available through the aquarium trade. We conclude that the spread of non-native crayfish introductions throughout Turkey will increase local problems, because introductions of non-native crayfish in many parts of the world have been known to have caused important reductions in population density and numbers of native crayfish species. Furthermore, freshwater ecosystems may be altered by such introductions and the economic viability of native crayfish species fisheries could be severely reduced in Turkey.     

Ecosystem of Caspian Sea threatened by pet-traded non-indigenous crayfish

Freshwater ecosystems are particularly vulnerable to biological invasions; the aquatic animal pet trade has been recognized as a significant pathway of introductions. Crayfish are considered a model group of traded organisms with a series of highly successful species already established in the wild, having the potential to negatively influence both indigenous crayfish species (ICS) as well as alter occupied ecosystems. Eastern Europe includes the entire native ranges of indigenous Astacus leptodactylus sensu lato and A. pachypus. This region has been largely overlooked and considered relatively safe from the adverse impacts of non-indigenous crayfish species (NICS). In this study, we evaluated the crayfish pet trade in the Lower Volga Region with special emphasis on Astrakhan, the biggest city of Russian Federation in the region located just in the delta of Volga River, thus being a potential gateway of introductions to the Caspian Sea and adjacent freshwaters. The local pet trade involves 12 NICS. Considering their origin, availability, probability of establishment, invasiveness and further aspects, Procambarus fallax f. virginalis, P. clarkii and Cherax destructor are considered potentially the most problematic, including transmission of diseases like crayfish plague caused by Aphanomyces astaci or white spot syndrome virus. Taking this information as a whole, the availability of NICS with a high probability of overlapping the entire range of European ICS means that attention is warranted. Further research is needed to corroborate the abilities of NICS and their associated diseases to withstand specific conditions of the Caspian Sea as well as the adjacent Black and Azov Seas, all possessing different degrees of elevated salinity.     

Risk assessment of the crayfish pet trade based on data from the Czech Republic

The pet trade in freshwater crustaceans, including crayfish, has grown rapidly in recent decades and become an important pathway for introducing new non-indigenous species into Europe. This paper provides the first overview of non-indigenous crayfish species (NICS) traded as ornamental and their potential impact in the Czech Republic, which is the second leading importer into Europe. The paper presents a full list of traded crayfish species, their market availability, and trade names or misnomers used in the country. In total, 27 crayfish species from all three families are advertised and marketed, of which Astacus astacus is the only indigenous species. Only three NICS were recognized as very common on the market. The invasiveness and risk associated with ornamental crayfish trade were assessed using the Freshwater Invertebrate Invasiveness Scoring Kit. Five NICS were classified into the high-risk category, the highest score being for Procambarus fallax f. virginalis. The invasiveness of crayfish indigenous to North America is significantly greater than that of crayfish from the rest of the world, and therefore regulation in this regard is recommended.     

Positive selection of beautiful invaders: long-term persistence and bio-invasion risk of freshwater crayfish in the pet trade

After interest in keeping crayfish (Crustacea, Decapoda, Astacida) in home aquaria peaked in the mid-2000s, the aquarium trade has become a novel introduction pathway for non-native crayfish species in Germany. Here, we provide an update on the ornamental crayfish trade approximately one decade after the ‘crayfish hype’ to explore the long-term implications in terms of bio-invasion risk. Specifically, species’ availability in e-commerce and potential invasiveness were assessed and compared to previous studies. Morphological and ecological traits of the offered species were compiled and related to their long-term availability (covering 2005–2015). In July 2015, a total of 31 online shops offered 28 crayfish species, which represents a decline of 24 % in species diversity compared to the late 2000s. The estimated rate of import of new species has considerably flattened and approaches pre-hype values (<1 species year^?1). However, the risk associated with the offered species, as assessed by a risk screening tool, has not decreased compared to the late 2000s. Long-term availability in the trade was primarily determined by bright coloration, the ability to reproduce under warm aquarium conditions, and a preference for lentic habitats. Species featuring such traits are likely to persist in the aquarium trade and include four high-risk species, most notably invasive and crayfish plague-carrying red swamp crayfish (Procambarus clarkii) and Marmorkrebs (Procambarus fallax f. virginalis). Persistent propagule pressure from aquaria has substantially contributed to the establishment of both species in Germany, stressing the need for more effective pathway management.     

Associations between stream habitat characteristics and native and alien crayfish occurrence

Human mediated introductions of non-indigenous crayfish species (NICS) are responsible for their rapid colonisation of European freshwaters. The introduction of North American crayfish is furthermore linked to the spread of crayfish plague and the decline of indigenous crayfish species (ICS). As the management of ICS and NICS have become necessary, a detailed knowledge on their distribution and ecological requirements is needed. We studied the current range of native noble crayfish Astacus astacus and stone crayfish Austropotamobius torrentium, as well as alien signal crayfish Pacifastacus leniusculus in Carinthia (Austria) and evaluated environmental and physical habitat features in streams with and without crayfish. Meanwhile, the loss of many ICS populations was recorded and alien P. leniusculus was found to be widespread in this region. Most of the habitat features of streams having crayfish differed significantly from sites lacking crayfish for at least one investigated native or alien species. Furthermore, multivariate and regression analyses showed specific differences in the habitat use of the investigated crayfish. Our results showed that the presence of alien P. leniusculus was associated with larger and smoother sloped lowland rivers, while the occurrence of the two native species was confined to smaller streams either at higher altitudes and with distinct physical habitat conditions (A. torrentium) or with moderate water temperatures (A. astacus). This study helps to identify potential refuge areas for the endangered native species and to predict the further spread of the most common non-native crayfish species in European streams.     

Invasion risks posed by the aquarium trade and live fish markets on the Laurentian Great Lakes

International trade is an important mechanism for global non-indigenous species introductions, which have had profound impacts on the biodiversity of aquatic ecosystems including the Laurentian Great Lakes. The best-documented vector by which non-indigenous species have entered the Great Lakes is ballast water discharged by transoceanic ships. A variety of potential alternative vectors exist, including the intentional release of aquarium or food organisms. To assess whether these vectors pose a significant invasion risk for the Great Lakes, we surveyed fish sold live in markets and fish, mollusks and macrophytes sold in pet and aquarium stores within the Great Lakes watershed. We evaluated invasion risk using information on species’ thermal tolerance, history of invasion elsewhere, and potential propagule loads as indicated by frequency of occurrence in shops. Our research suggests that both the aquarium industry and live fish markets represent potential sources of future invaders to the Great Lakes, including several aquarium fishes and macrophytes, as well as Asian carp species sold in fish markets. Currently, few regulatory mechanisms exist to control these potential vectors.     

A risk assessment of aquarium trade introductions of seaweed in European waters

Aquaculture and maritime traffic have been identified as the main vectors for introductions of alien marine species. Except for one notorious case of Caulerpa taxifolia, the role of aquarium trade towards the introduction of alien seaweeds has been largely unassessed. Here, we address the risk of accidental release of seaweed species from the aquarium trade market in European waters. We assessed the importance and diversity of seaweed species in the European online aquarium retail circuit. Our web survey revealed more than 30 genera available for online sale into Europe, including known introduced and invasive species. A second aspect of the study consisted in sampling algal diversity found in aquaria. While allowing direct and accurate identification of the specimens, this approach was targeting not only ornamental species, but also seaweeds that may be accidentally present in the aquarium circuit. By DNA-barcoding we identified no less than 134 taxa, 7 of which are flagged as introduced in Europe and 5 reported as invasive. Climate envelope models show that at least 23 aquarium species have the potential to thrive in European waters. As expected by the tropical conditions in most aquaria, southern Atlantic regions of Europe and the Mediterranean are the most vulnerable towards new introductions. Further predictions show that this risk will increase and shift northwards as global warming proceeds. Overall our data indicate that aquarium trade poses a potential risk of new seaweed introductions, and calls for a cautious approach.     

Neither variation loss,nor change in selfing rate is associated with the worldwide invasion of Physa acuta from its native North America

Whether bioinvasions are associated with a loss of genetic diversity and a change in mating system is instrumental for understanding the evolutionary fate of invasive species. Little loss is expected under strong propagule pressure which might be a general situation in widespread, efficient invader. In hermaphroditic species, we have few examples of a transition between outcrossing and selfing as a consequence of invasion, though this is classically predicted (as a corollary to Baker’s law). We estimated microsatellite variation in 44 populations of the widespread freshwater snail Physa acuta sampled at worldwide scale (including several populations from its native North America). Neither loss of variation (or bottleneck), nor increase in selfing rate was detected in invaded areas. Moreover there was no isolation by distance at large geographic scale, and limited geographic coherence in genetic patterns was detected using STRUCTURE software—the West Mediterranean area being an exception. Such patterns might be explained by (1) multiple introductions in the invaded areas, presumably fostered by aquarium trade, followed by regional spread in some cases—in which case mating partners might be numerous enough to prevent transition towards higher selfing rates, and (2) invasions from the whole native area. This suggests that P. acuta is an exceptionally efficient invader (which is not true of related species), but the reasons of its success remain elusive.     

Introduction history of non-native freshwater fish in Okinawa-jima Island: ornamental aquarium fish pose the greatest risk for future invasions

We examined the introduction history of non-native freshwater fish in Okinawa-jima Island, Japan, to identify the pathway posing the greater risk for future invasions and to measure the strength of ornamental fish introductions as a vector of new invasions using all available records of freshwater fish introductions to date. At least 45 non-native freshwater fish have been introduced to Okinawa-jima Island. Of those, 22 species have successfully established in natural waters and, consequently, non-native fish species represent 76 % of the total freshwater fish fauna. The most important pathway was via the dumping of unwanted ornamental aquarium fish, which accounted for 71 % of the total introductions. The introduction of ornamental fish has occurred extensively in recent decades, and all fish introduced since the 1980s have been ornamental aquarium fish. The overall rate of establishment success was estimated at 51 %, although this is undoubtedly an overestimate because of unreported failed introductions. Establishment rates varied between stocked fish (100 %) and dumped ornamental fish (39 %), which may reflect the low propagule pressure of ornamental fish. From the observed trends in freshwater fish introductions, the dumping of ornamental fish into natural waters is expected to continue if no action is taken to reduce this most important pathway. We recommend regulations against the release of unwanted pet fish into natural waters, better programs for returning unwanted pet fish to stores or local zoos, educational programs for aquarists and retailers, and regulations against selling and trading ornamental fish that are judged to pose a high risk of causing economic or ecological harm.     

Temporal trends in non-indigenous freshwater species records during the 20th century: a case study in the Iberian Peninsula

Galicia (NW Spain) is a region with a high number of freshwater endemics, and probably the best preserved area concerning fish populations in the Iberian Peninsula, where records of non-indigenous freshwater species are recent when compared to the rest of the Peninsula. Detailed analysis of introductions of those species with records after 1900 present in both areas shows that delays were up to 100 years for species introduced on the Iberian Peninsula at the beginning of the twentieth century, but the tendency adjust to a decreasing linear regression, with species introduced after 1995 being almost immediately present in Galicia. We underline the outstanding role of aquarium trade on these results. Analysis of temporal trends highlights several periods with numerous introductions, and shows a different trend in the last decade depending on the group of organisms, with a clear deceleration in introduction rates of vertebrates, but a continuous growing trend for invertebrates. Recent educational programs might be responsible for the reduction in the inflow of vertebrates, but there is still a need for the control of less conspicuous but equally harmful invertebrates and plants, as it will take longer to make both stakeholders and public aware of their detrimental effects on their new habitats.     

First records of the non-indigenous signal crayfish (<Emphasis Type="Italic">Pacifastacus leniusculus</Emphasis>) and its threat to noble crayfish (<Emphasis Type="Italic">Astacus astacus</Emphasis>) populations in Estonia

This study gives an overview of status and distribution of signal crayfish (Pacifastacus leniusculus), the first NICS in Estonia and its influence on native noble crayfish (Astacus astacus) populations. The first specimen of signal crayfish was caught during the monitoring of noble crayfish in North Estonia in 2008. The signal crayfish has since been found in three additional sites. Test fishing has indicated that the abundance of signal crayfish has been fluctuating between years and among localities. It has had strong negative impact on abundance of one noble crayfish population. The disconnected distribution of signal crayfish strongly suggests that these populations are the result of human-assisted introductions. Real-time PCR analyses proved that signal crayfish carry the causative agent of the crayfish plague, an oomycete Aphanomyces astaci, thus contributing to its spread. Mortalities in noble crayfish populations had been caused by A. astaci strains from A, B and E genotype group.     

Aquarium molluscs as a case study in risk assessment of incidental freshwater fauna

Because biological invasions may cause loss of biodiversity, accurate predictions are necessary for implementing effective restrictions aimed at specific high-risk taxa. The majority of freshwater macroinvertebrate invaders are molluscs and crustaceans. The pet trade has been considered one of the main pathways for new introductions of such species. Risk assessment is usually focused on traded ornamental species whereas, despite their potential importance, incidental “hitchhiking” molluscs are usually given only minimal consideration. We surveyed the Czech Republic, which is one of the leading markets for aquarium species in the European Union (EU), and found 41 freshwater mollusc species (25 ornamental gastropods, 6 ornamental clams, and 10 “hitchhiking” gastropods) representing 13 families. We extrapolated data from the Czech Republic and, using Climatch v. 1.0, matched the climate in each species’ native range to the entire territory of the EU. We also assessed the risk associated with each species by FI-ISK. “Hitchhiking” gastropods were found to be significantly more hazardous and with higher potential to become established within the EU than were ornamental gastropods and bivalves. Many “hitchhikers” may be easily overlooked due to their small size and cryptic coloration or shape. Thus, they easily can be accidentally imported in association with aquarium plants. Therefore, we recommend here to disinfect imported ornamental plants to eradicate these unwanted faunal assemblages.     

Aquarium hitchhikers: attached commensals imported with freshwater shrimps via the pet trade

The keeping of home aquaria is one of the most popular hobbies globally. In contrast to the ornamental fish trade, decapod crustaceans such as shrimps, crayfish and crabs are relatively new to the pet trade. Nevertheless, the popularity of ornamental shrimp in freshwater aquaria has rapidly increased in recent years. Indonesia is one of the leading producers and exporters of ornamental aquatic animals globally and the Czech Republic is a gateway for these animals into the European Union territory. The pathway for introductions of organisms unintentionally moved in association with ornamental shrimps via the international trade has to date not been evaluated. We examined a small number of shrimps imported from Indonesia into the Czech Republic in May 2015 and found large numbers of the protozoan Vorticella sp., one species of scutariellid temnocephalidan (Caridinicola sp.), and one species of bdelloid rotifer, associated with two species of atyid shrimps, indicating an invasion risk from fauna carried unintentionally by this vector. Although our observations were limited in scale, we estimate the total number of commensal fauna imported into the Czech Republic with ornamental shrimps via the pet trade to be in the order of hundreds of thousands per month. As attached organisms can directly or indirectly cause diseases in certain species of decapod crustaceans, we recommend five steps to reduce risks of introduction of “hitchhikers” to aquaria and wildlife.     

175 Toward an Optical Biogeography of the Oceans

Invasions of marine communities by seaweeds are increasing globally. Vectors for introductions are primarily aquaculture and the aquarium trade. Attention to these vectors has been minimal, and few, if any, regulations exist to prevent seaweed introductions. Challenges in preventing, eradicating, and controlling invasive seaweeds will be discussed using the invasion of Caulerpa taxifolia in southern California as a model.     

Loopholes in the regulation of invasive species: genetic identifications identify mislabeling of prohibited aquarium plants

Numerous invasive aquatic species introductions can be traced to the aquarium trade. Many potentially harmful aquarium species may be difficult to identify based on morphology alone. As such, some prohibited or invasive species may be available for purchase if they are mislabeled as species without restrictions. Here we compare molecular identifications to internet vendors’ identifications for accessions of a popular genus of aquarium plants that are difficult to distinguish morphologically (Myriophyllum; watermilfoils). Specifically, we identified the extensive mislabeling of M. heterophyllum—an invasive species in the northeastern and western US. Furthermore, genotypes of M. heterophyllum found in our aquarium survey have also been found in invasive populations, suggesting their potential introduction through escape from aquaria, water gardens, or nurseries. Two additional taxa were sold under incorrect names. Finally, our survey revealed that Myriophyllum taxa present in the aquarium trade generally have poorly known distributions and ecologies, and therefore their invasive potential is unknown. Our study confirms that molecular identification methods can provide a valuable tool to survey commercial pathways for potentially harmful species that are otherwise difficult to identify.     

Historical,human, and environmental drivers of genetic diversity in the red swamp crayfish (Procambarus clarkii) invading the Iberian Peninsula

1. Patterns of genetic diversity in invasive populations can be modulated by a range of factors acting at different stages of the invasion process, including the genetic composition of the source population(s), the introduction history (e.g. propagule pressure), the environmental suitability of recipient areas, and the features of secondary introductions.
2. The North American red swamp crayfish, Procambarus clarkii, is one of the most widely introduced freshwater species worldwide. It was legally introduced into Spain twice, near the city of Badajoz in 1973 and in the Guadalquivir marshes in 1974. Thereafter the species rapidly colonised almost the entire Iberian Peninsula.
3. We used seven nuclear microsatellites to describe the genetic diversity and structure of 28 locations distributed across the Iberian Peninsula and to explain the expansion process of the red swamp crayfish. Additionally, we analysed the relationship between environmental suitability and genetic diversity of the studied locations.
4. The red swamp crayfish had a clear spatial genetic structure in the Iberian Peninsula, probably determined by the two independent introduction events in the 1970s, which produced two main clusters separated spatially, one of which was dominant in Portugal and the other in Spain.
5. The human-mediated dispersal process seemed to have involved invasion hubs, hosting highly genetically diverse areas and acting as sources for subsequent introductions. Genetic diversity also tended to be higher in more suitable environments across the Iberian Peninsula .
6. Our results showed that the complex and human-mediated expansion of the red swamp crayfish in the Iberian Peninsula has involved several long- and short-distance movements and that both ecological and anthropogenic factors have shaped the genetic diversity patterns resulting from this invasion process. Early detection of potential invasion hubs may help to halt multiple short-distance translocations and thus the rapid expansion of highly prolific invasive species over non-native areas.

     

Freshwater crayfish invasions in South Africa: past,present and potential future

Freshwater crayfish invasions have been studied around the world, but less so in Africa, a continent devoid of native freshwater crayfish. The present study reviews historical and current information on alien freshwater crayfish species introduced into South Africa and aims to indicate which areas are at risk from invasion. As is the case elsewhere, South Africans have shown a keen interest in both farming and keeping freshwater crayfish as pets, which has resulted in Cherax cainii, Cherax destructor, Cherax quadricarinatus and Procambarus clarkii being introduced to the country. There is evidence of successful establishment in the wild for C. quadricarinatus and P. clarkii in different parts of the country. Species distribution models suggest that the eastern part of the country and parts of the Eastern and Western Cape are at higher risk of invasion. At present, illegal translocations represent the most likely pathway of crayfish spread in South Africa. A continued risk of invasion by freshwater crayfish species in South Africa is highlighted, which reinforces the need for more research, as well as for strong mitigation measures, such as stronger policing of existing regulations, management or eradication where feasible and public education.     

173 Challenges in Preventing,Eradicating, and Controlling Invasive Seaweeds: The Southern California Invasion of Caulerpa Taxifolia as a Model

Invasions of marine communities by seaweeds are increasing globally. Vectors for introductions are primarily aquaculture and the aquarium trade. Attention to these vectors has been minimal, and few, if any, regulations exist to prevent seaweed introductions. Challenges in preventing, eradicating, and controlling invasive seaweeds will be discussed using the invasion of Caulerpa taxifolia in southern California as a model.