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.     

Analysis of the marine ornamental fish trade at Ceará State, northeast Brazil

Brazil is one of the leading exporters of ornamental fishes, mostly freshwater; however, monitoring of the trade is nearly non-existent in the country. This paper provides an initial assessment of a new venture, the marine aquarium fish trade at Ceará State, northeast Brazil, aiming to document the species traded, to provide preliminary estimates of numbers of specimens traded, and to identify priorities in data collection and monitoring. A total of 143 species and 199 304 fishes were traded. From the total, 109 species were native and represented 84% of the fishes traded. Thirty-four exotic species figured on the permits and amounted to nearly 16% of the exports; however, most of them consist of misidentified native species. Nearly 90% of the fish trade was directed to the international market. Official figures represent an underestimation of the total number of captured specimens.     

Opportunities for public aquariums to increase the sustainability of the aquatic animal trade

The global aquatic pet trade encompasses a wide diversity of freshwater and marine organisms. While relying on a continual supply of healthy, vibrant aquatic animals, few sustainability initiatives exist within this sector. Public aquariums overlap this industry by acquiring many of the same species through the same sources. End users are also similar, as many aquarium visitors are home aquarists. Here we posit that this overlap with the pet trade gives aquariums significant opportunity to increase the sustainability of the trade in aquarium fishes and invertebrates. Improving the sustainability ethos and practices of the aquatic pet trade can carry a conservation benefit in terms of less waste, and protection of intact functioning ecosystems, at the same time as maintaining its economic and educational benefits and impacts. The relationship would also move forward the goal of public aquariums to advance aquatic conservation in a broad sense. For example, many public aquariums in North America have been instrumental in working with the seafood industry to enact positive change toward increased sustainability. The actions include being good consumers themselves, providing technical knowledge, and providing educational and outreach opportunities. These same opportunities exist for public aquariums to partner with the ornamental fish trade, which will serve to improve business, create new, more ethical and more dependable sources of aquatic animals for public aquariums, and perhaps most important, possibly transform the home aquarium industry from a threat, into a positive force for aquatic conservation.     

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.     

The aquarium trade as a potential source of fish introductions in southwestern Europe

The aquarium trade has been identified as an important vector of aquatic invasive species but this question has mostly been investigated in North America. We investigated the variation in diversity and species composition in different trade types in southwestern Europe (three major international wholesalers, different retail store types, and local internet forums), mostly in Spain and Portugal. As in previous studies, the diversity of fishes in the aquarium trade was vast, with a total of 20 orders, 79 families, and 1,133 fish species detected in the trade types analyzed. 248 species were observed in a single metropolitan area (Barcelona), with estimates of about 294 species being present. International wholesalers had higher species richness and evenness, with a single one having over 700 species. General pet stores had much lower evenness but due to high turnover had a total richness of over 200 species. Internet forums had the lowest evenness but similar richness. The different commerce types varied significantly in relative species abundance with about a dozen of popular fish species (e.g., goldfish, Siamese fighting fish, common carp, guppy, swordtails) dominating the retail stores, particularly the general pet stores. Our results imply that frequency in the trade varies strongly among species and commerce types and although general pet stores have usually low diversity, this is compensated with a higher species turnover. Many of the most popular species are well known invasive species and some of the species available are temperate species that might establish in Europe, reinforcing the need for more careful implementation of education programs, regulation and monitoring of trade, and internalization of environmental costs by the industry.     

Understanding the United Kingdom marine aquarium trade – a mystery shopper study of species on sale

In this study, we conducted a unique survey of marine ornamental fishes appearing in UK retail stores, as well as a review of government trade statistics, with the aim to significantly strengthen the evidence-base in support of future management initiatives. Fifty marine aquarium retailers were visited. A total of 380 marine aquarium fish species (4926 individuals), from 48 families were recorded with the largest proportion of individuals belonging to the families Pomacentridae, Acanthuridae, Apogonidae, Labridae, Pomacanthidae, Gobiidae and Labridae. The majority of fishes for sale (91% of species) originated from the Indo-Pacific Ocean, with only a small number (9% of species) derived from the Atlantic Ocean. However, exact sources of individual species were unclear and poorly documented. Government trade statistics revealed that the ornamental reef-fish trade in the UK grew markedly between 1996 and 2008 with a rapid acceleration in 2003–2004. However, imports have declined since 2008 and amounted to less than 305,000 kg in 2017 with an economic value of UK £3 million (c. US $3.8). Recent trade data (2017) identify Indonesia, USA, Philippines and the Maldives as the most important countries in terms of imports to the UK. The UK is an important exporter of wild-caught fishes via trans-shipment, but also production of tank-reared animals. Several species observed for sale in the UK have been designated by the IUCN and CITES as being of conservation concern, although all these animals are thought to have been captive-reared.     

The importance of the marine ornamental reef fish trade in the wider Caribbean

The marine ornamental fish trade began in the 1930s in Sri Lanka, spread to Hawaii and the Philippines in the 1950s, and expanded to a multi-million dollar industry in the 1970s with fisheries established throughout the tropical Pacific, Indian and Atlantic Oceans. Currently, 45 countries supply global markets an estimated 14-30 million fish annually, with an import value of US$28-44 million. The largest suppliers are Indonesia and the Philippines, followed by Brazil, Maldives, Vietnam, Sri Lanka and Hawaii. In the tropical Western Atlantic, 16 countries have export fisheries, including the U.S. (Florida and Puerto Rico). The U.S. is the world's largest buyer, followed by the European Union and Japan. The global trade consists of over 1400 species of reef fishes, of which only about 25 are captive bred on a commercial scale. Damselfish, anemonefish, and angelfish constitute over 50% of the global volume; butterflyfish, wrasses, blennies, gobies, triggerfish, filcfish, hawkfishes, groupers and basselets account for 31% of the trade, and the remaining 16% is represented by 33 families. The most important fishes from the Caribbean are angelfish (six species), seahorses (two species), royal gramma, jawfish, queen triggerfish, redlip blenny, puddingwife, bluehead wrasse, and blue chromis. The Caribbean currently supplies a small percentage of the global trade in marine ornamental species, but ornamental fisheries in this region represent important emerging industries. It is critical that effective ornamental fishery management plans and regulations are developed and enforced, and fishery-dependent and fishery-independent data are collected and utilized in decision making processes to ensure sustainable ornamental fisheries throughout the region.     

Barcoding and border biosecurity: identifying cyprinid fishes in the aquarium trade

Background

Poorly regulated international trade in ornamental fishes poses risks to both biodiversity and economic activity via invasive alien species and exotic pathogens. Border security officials need robust tools to confirm identifications, often requiring hard-to-obtain taxonomic literature and expertise. DNA barcoding offers a potentially attractive tool for quarantine inspection, but has yet to be scrutinised for aquarium fishes. Here, we present a barcoding approach for ornamental cyprinid fishes by: (1) expanding current barcode reference libraries; (2) assessing barcode congruence with morphological identifications under numerous scenarios (e.g. inclusion of GenBank data, presence of singleton species, choice of analytical method); and (3) providing supplementary information to identify difficult species.

Methodology/Principal Findings

We sampled 172 ornamental cyprinid fish species from the international trade, and provide data for 91 species currently unrepresented in reference libraries (GenBank/Bold). DNA barcodes were found to be highly congruent with our morphological assignments, achieving success rates of 90–99%, depending on the method used (neighbour-joining monophyly, bootstrap, nearest neighbour, GMYC, percent threshold). Inclusion of data from GenBank (additional 157 spp.) resulted in a more comprehensive library, but at a cost to success rate due to the increased number of singleton species. In addition to DNA barcodes, our study also provides supporting data in the form of specimen images, morphological characters, taxonomic bibliography, preserved vouchers, and nuclear rhodopsin sequences. Using this nuclear rhodopsin data we also uncovered evidence of interspecific hybridisation, and highlighted unrecognised diversity within popular aquarium species, including the endangered Indian barb Puntius denisonii.

Conclusions/Significance

We demonstrate that DNA barcoding provides a highly effective biosecurity tool for rapidly identifying ornamental fishes. In cases where DNA barcodes are unable to offer an identification, we improve on previous studies by consolidating supplementary information from multiple data sources, and empower biosecurity agencies to confidently identify high-risk fishes in the aquarium trade.     

Marine Ornamental Trade in Brazil

Brazil is one of the five leading exporting countries of tropical aquarium fishes in the world, and the interest in marine ornamental organisms has increased substantially there from the mid to the late 1990s. About 120 reef fish species are currently harvested in Brazil's ornamental trade. Among the 75 most harvested species, 26 (34.7%) are endemic, eight (10.7%) are rare, and six (8.2%) are estuarine-dependent species. Fifty-five species (75.3%) have complex reproductive strategies and/or parental care. In quantitative terms, the top 10 species comprises 62% of the species exported from Brazil to the USA and the European Community. The most harvested reef invertebrates include about 65 species. The most representative groups are crustaceans with 15 species (23%), and molluscs and stony corals with 10 species (15.4%) each. Among these, 15 (23%) are endemics, nine (13.8%) are rare species, and seven (10.8%) are important reef builders. A case of local extinction of the giant anemone Condylactis gigantea is reported. To alleviate ecological impacts a series of urgent measures is suggested, including the creation of specific laws for marine ornamental harvesting and improving law enforcement to prevent illegal trade in Brazil.     

The ornamental fish trade and fish conservation

The global trade in ornamental fish and associated aquarium and pond accessories is in excess of U.S. $7 × 10⁹ each year. Although the majority of freshwater fish involved in the trade are from captive-bred sources, significant numbers are still removed from the wild. In addition, almost all of the marine fish in the trade are wild-caught. Whilst habitat destruction, pollution and overfishing for food are the main threats facing fish populations in the wild, the ornamental fish trade may have adverse effects as a result of the introduction of nonnative organisms, and by the direct depletion of wild stocks. The ornamental fish trade is ideally placed to raise public awareness of, and actively support, fish conservation efforts, and must maintain a close liaison with legislative-forming organizations seeking to impose further trade restrictions.     

DNA barcoding of South Africa’s ornamental freshwater fish – are the names reliable?

Trade in freshwater ornamental fish in South Africa is currently regulated by a ‘blacklist’ to prevent potentially invasive taxa from establishing in the country. Because its effective implementation requires accurate identification, the aim of the present study was to test whether DNA barcoding is a useful tool to identify freshwater fishes in the South African pet trade. A total of 351 aquarium fish specimens, representing 185 traded taxa, were sequenced for the mitochondrial COI barcoding marker in 2011 and 2012. Lake Malawi cichlids were treated as a single group due to a lack of resolution in their COI marker, resulting in a data set of 137 successfully sequenced taxa. The Barcode Of Life Database (BOLD) and GenBank were used for taxonomic assignment comparisons. The genetic identification matched the scientific name inferred from the trade name for 60 taxa (43.8%) using BOLD, and for 67 taxa (48.9%) using GenBank. A genetic ID could not be assigned in 47 (34.3%) cases using BOLD and in 37 cases (27%) using GenBank. Whereas DNA barcoding can be a useful tool to help identify imported freshwater fishes, it requires further development of publicly available databases to become a reliable means of identification.     

Online auction marketplaces as a global pathway for aquatic invasive species

Hydrobiologia - The ornamental aquarium pet trade is a leading pathway for the introduction of aquatic invasive species. In addition to purchasing live organisms in stores, hobbyists are engaging...     

Invasive aquarium fish transform ecosystem nutrient dynamics

Trade of ornamental aquatic species is a multi-billion dollar industry responsible for the introduction of myriad fishes into novel ecosystems. Although aquarium invaders have the potential to alter ecosystem function, regulation of the trade is minimal and little is known about the ecosystem-level consequences of invasion for all but a small number of aquarium species. Here, we demonstrate how ecological stoichiometry can be used as a framework to identify aquarium invaders with the potential to modify ecosystem processes. We show that explosive growth of an introduced population of stoichiometrically unique, phosphorus (P)-rich catfish in a river in southern Mexico significantly transformed stream nutrient dynamics by altering nutrient storage and remineralization rates. Notably, changes varied between elements; the P-rich fish acted as net sinks of P and net remineralizers of nitrogen. Results from this study suggest species-specific stoichiometry may be insightful for understanding how invasive species modify nutrient dynamics when their population densities and elemental composition differ substantially from native organisms. Risk analysis for potential aquarium imports should consider species traits such as body stoichiometry, which may increase the likelihood that an invasion will alter the structure and function of ecosystems.     

Current status of sperm cryopreservation in biomedical research fish models: zebrafish, medaka, and Xiphophorus

Aquarium fishes are becoming increasingly important because of their value in biomedical research and the ornamental fish trade, and because many have become threatened or endangered in the wild. This review summarizes the current status of sperm cryopreservation in three fishes widely used in biomedical research: zebrafish, medaka, and live-bearing fishes of the genus Xiphophorus, and will focus on the needs and opportunities for future research and application of cryopreservation in aquarium fish. First, we summarize the basic biological characteristics regarding natural habitat, testis structure, spermatogenesis, sperm morphology, and sperm physiology. Second, we compare protocol development of sperm cryopreservation. Third, we emphasize the importance of artificial fertilization in sperm cryopreservation to evaluate the viability of thawed sperm. We conclude with a look to future research directions for sperm cryopreservation and the application of this technique in aquarium species.     

Where are they all from? – sources and sustainability in the ornamental freshwater fish trade

The global trade in ornamental fish involves c. 125 countries worldwide and is worth c. US $15–30 billion each year. This total is dominated (90%) by freshwater fishes, most of which are sourced from breeding facilities located in developing countries, typically in Asia or South America, but also in Israel, USA and Europe. Some fish are still obtained from natural (wild) sources, but the exact percentage of wild-caught fish is difficult to quantify given a lack of reliable data. Although c. 1000 species of freshwater fishes are widely available (from a total of > 5300 on sale), the most dominant freshwater fishes in the market comprise only 30 species from the orders Cyprinodontiformes, Perciformes, Characiformes and Siluriformes. In this perspectives review paper, illustrative example case studies of wild-fish collecting (Barcelos and Rio Xingu, Brazil) and breeding projects (Java, Indonesia) are described. In addition, wild-collecting expeditions to West Papua, Indonesia are discussed, focused on discovering novel species of rainbowfish (Melanotaeniidae) for breeding in captivity. Sustainability of the aquarium industry is considered in its broadest sense. The aquarium industry has been portrayed as both a major threat to natural ecosystems, but also as being part of the solution in terms of helping to maintain species when they have gone extinct in the wild or offering an income to impoverished citizens who might otherwise engage in much more destructive practices.     

Tackling aquatic invasions: risks and opportunities for the aquarium fish industry

The aquarium trade is an important and rapidly growing vector for introduced species in the United States. We examined this vector by surveying pet stores in the San Francisco Bay–Delta region to compile a list of aquarium fish species commonly stocked. We identified which of these species might be able to survive in the Bay–Delta, and investigated store representatives’ knowledge and attitudes about biological invasions. A restrictive analysis using conservative estimates of fish temperature tolerances and environmental conditions found that the local aquarium trade includes 5 fish species that can survive in a temperate system such as the Bay–Delta. Under more inclusive parameters, up to 27 fish species met the criteria for survival in the Bay–Delta. We further explored these results by comparing potential invader incidence between different types of stores. In the more restrictive analysis, three national retail chains stocked significantly more potentially invasive species than independent aquarium stores, but there was no difference in the more inclusive analysis. A significantly higher percentage of fish taxa were easily identifiable and well-labeled in chain stores than in independent stores. Most aquarium store representatives indicated willingness to take action to reduce the threat of trade-related introductions, although chain store employees were more willing to assign responsibility for reducing this threat to the aquarium industry than were independent store employees. Management efforts for this vector should focus on (a) improving labeling and identification of fish species in stores, (b) expanding the often spotty data on fish physiological tolerances, especially for saltwater species, (c) educating customers and store employees about the risks posed by pet release, and (d) providing better options for responsible disposal of unwanted fish. Electronic Supplementary Material   The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Stress and welfare in ornamental fishes: what can be learned from aquaculture?

The ornamental fish trade is estimated to handle up to 1·5 billion fishes. Transportation and handling of fishes imposes a range of stressors that can result in mortality at rates of up to 73%. These rates vary hugely, however, and can be as low as 2%, because they are generally estimated rather than based on experimental work. Given the numbers of ornamental fishes traded, any of the estimated mortality rates potentially incur significant financial losses and serious welfare issues. Industry bodies, such as the Ornamental Aquatic Trade Association (OATA), have established standards and codes of best practice for handling fishes, but little scientific research has been conducted to understand the links between stress, health and welfare in ornamental species. In aquaculture, many of the same stressors occur as those in the ornamental trade, including poor water quality, handling, transportation, confinement, poor social and physical environment and disease and in this sector directed research and some resulting interventions have resulted in improved welfare standards. This review considers the concept of welfare in fishes and evaluates reported rates of mortality in the ornamental trade. It assesses how the stress response can be quantified and used as a welfare indicator in fishes. It then analyses whether lessons from aquaculture can be usefully applied to the ornamental fish industry to improve welfare. Finally, this analysis is used to suggest how future research might be directed to help improve welfare in the ornamental trade.     

Pyrosequencing Reveals Diverse and Distinct Sponge-Specific Microbial Communities in Sponges from a Single Geographical Location in Irish Waters

Marine sponges are host to numerically vast and phylogenetically diverse bacterial communities, with 26 major phyla to date having been found in close association with sponge species worldwide. Analyses of these microbial communities have revealed many sponge-specific novel genera and species. These endosymbiotic microbes are believed to play significant roles in sponge physiology including the production of an array of bioactive secondary metabolites. Here, we report on the use of culture-based and culture-independent (pyrosequencing) techniques to elucidate the bacterial community profiles associated with the marine sponges Raspailia ramosa and Stelligera stuposa sampled from a single geographical location in Irish waters and with ambient seawater. To date, little is known about the microbial ecology of sponges of these genera. Culture isolation grossly underestimated sponge-associated bacterial diversity. Four bacterial phyla (Actinobacteria, Bacteroidetes, Firmicutes, Proteobacteria) were represented amongst ~200 isolates, compared with ten phyla found using pyrosequencing. Long average read lengths of ~430 bp (V1-V3 region of 16S rRNA gene) allowed for robust resolution of sequences to genus level. Bacterial OTUs (2,109 total), at 95% sequence similarity, from ten bacterial phyla were recovered from R. ramosa, 349 OTUs were identified in S. stuposa representing eight phyla, while 533 OTUs from six phyla were found in surrounding seawater. Bacterial communities differed significantly between sponge species and the seawater. Analysis of the data for sponge-specific taxa revealed that 2.8% of classified reads from the sponge R. ramosa can be defined as sponge-specific, while 26% of S. stuposa sequences represent sponge-specific bacteria. Novel sponge-specific clusters were identified, whereas the majority of previously reported sponge-specific clusters (e.g. Poribacteria) were absent from these sponge species. This deep and robust analysis provides further evidence that the microbial communities associated with marine sponge species are highly diverse and divergent from one another and appear to be host-selected through as yet unknown processes.     

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.