Small size today , aquarium dumping tomorrow : sales of juvenile non-native large fish as an important threat in Brazil

Informal sales of large-bodied non-native aquarium fishes (known as “tankbusters”) is increasing among Brazilian hobbyists. In this study, we surveyed this non-regulated trade on Facebook® from May 2012 to September 2016, systematically collecting information about the fishes available for trading: species, family, common/scientific names, native range, juvenile length, behavior, number of specimens available in five geographical regions from Brazil. We also assessed the invasion risk of the most frequently sold species using the Fish Invasiveness Screening Test (FIST). We found 93 taxa belonging to 35 families. Cichlidae was the dominant family, and most species were native to South America. All species are sold at very small sizes (< 10.0 cm), and most display aggressive behavior. The hybrid Amphilophus trimaculatus × Amphilophus citrinellus, Astronotus ocellatus, Uaru amphiacanthoides, Osteoglossum bicirrhosum, Cichla piquiti, Pangasianodon hypophthalmus, Datnioides microlepis and Cichla kelberi were the main species available. The southeast region showed the greatest trading activity. Based on biological traits, the FIST indicated that Arapaima gigas, C. kelberi and C. temensis are high-risk species in terms of biological invasions via aquarium dumping. We suggest management strategies such as trade regulations, monitoring, euthanasia and educational programs to prevent further introductions via aquarium dumping.


Introduction
Fishkeeping is a worldwide hobby appretiated by people of all ages (CBD, 2010).It has been shown that aquarium keeping improves human well-being in many aspects, e.g. the development of responsibility in children (Edwards, Beck, 2002), reduction of stress levels in adults, and improved physical and psychological well-being in the elderly (Reaser, Meyers, 2007).The United States is the leading country in the number of hobbyists, with about 20 million enthusiasts (Chapman, 2000).Estimates indicate that american homes have 151.6 million ornamental fishes (APPMA, 2008), followed by the United Kingdom, with 140 million fishes (Marine & Coastal Committee, 2005).In Brazil, it is a growing hobby with 26 million fishes belonging to more than 300 species, being the second most frequent pet (AquaA3, 2015).
In order to understand this non-regulated market and the environmental risks associated, this study evaluated the sales of juvenile non-native large fish (JNLF, hereafter) among Brazilian hobbyists, via face-to-face personal contacts.So far, the importance of this new vector had not been evaluated consistently in Brazil, an here we present an overview of species available for trading, quantity, sizes, origin and ecological information related to their invasion risk.Based on this data, we discuss management strategies to prevent further invasions into Brazilian water bodies via aquarium dumping.

Material and Methods
Data sampling.We surveyed the informal ornamental trade in the Facebook ® (www.facebook.com)from May-2012 to September-2016.Ten hobbyist groups (i.e, exclusive sale groups of ornamental large fishes) were chosen randomly using standardized keywords (e.g.jumbo fishes, jumbo fish sales, jumbo cichlids, Brazil jumbo fishes, jumbo fishkeepers, keeping large fish, Central American cichlids) and monitored four times every month (once a week in the same day).To conduct the monitoring, one researcher (A.L.B.Magalhães) became a member of the group but did not contact any hobbyist during the period, so the trading process was not disturbed.The trade operates as follows: the hobbyist announces the species showing a picture, common or scientific name, juvenile length, price (Real currency) and location.When the purchase is agreed, hobbyists schedule to meet and complete the deal in privacy.
To determine the availability of JNLF for sale, we surveyed only fish species with maximum adult lengths above 20 cm.When a hobbyist announced the same species in more than one group, replicates were discarded.From the ten Facebook ® aquarium groups, we recorded information about the fishes on sale: length, number of specimens and geographical availability, considering 11 large urban centers of the north (Belém), northeast (São Luís, Fortaleza, João Pessoa, Recife, Salvador), mid-west (Brasília), southeast (Belo Horizonte, Rio de Janeiro, São Paulo), and south (Curitiba) regions of Brazil (Fig. 1).In addition, the family, common/scientific names, native range, maximum adult length and aggressiveness of these species were consulted in Axelrod (1992), Sandford, Crow (1996), Axelrod et al. (2005)   Data analysis.We calculated the total number of species available in the market, and according to families and native origin.We also calculated specimens availability, for each species and geographical region.The Kruskal-Wallis nonparametric analysis of variance (Sokal, Rohlf, 1995) was used to test differences in mean length between juvenile fishes on sale and their maximum lengths when adults.This test considered only the 15 most frequently available (announced for sale) species, which were pooled across species to test overall differences in length.

Results
We encountered sales of 93 taxa of JNLF, being 89 valid species and four hybrids (Appendix S1 -Available only as online supplementary file accessed with the online version of the article at http://www.scielo.br/ni).These taxa belonged to 35 families, native to six continents and one region.Among the families, Cichlidae was the dominant (34 species), followed by Polypteridae, Loricariidae and Cyprinidae (four species each).Potamotrygonidae, Osteoglossidae, Notopteridae and Serrasalmidae were represented by three species, while the remaining were represented by two or one species (Fig. 2).According to their native origin, 43 species (46.24%) were native to South America, especially the Amazon region (36.56%),followed by Africa and Asia (17.20% each), Central America (11.83%),North America (4.30%),Oceania (2.15%) and Caribbean (1.08%) (Fig. 3).The mean length of juvenile fish on sale was significantly lower than their maximum lengths (Fig. 4a).JNLF are able to reach (on average) 7.5 times their sizes at retail, and they are usually sold with ca.20% of their maximum lengths (Fig. 4b).All species are sold at very small sizes (< 10.0 cm on average), and some show contrasting lengths if compared to their maximum adult length, such as Cichla temensis, Lepisosteus oculatus, Osteoglossum bicirrhosum (Cuvier, 1829), Pangasianodon hypophthalmus and A. gigas (Fig. 4c).
The number of specimens traded among the ten hobbyist groups averaged 10.5 individuals/species, considering the entire study period.The main species available were (Tab.The risk assessment (FIST) for potential biological invasion via aquarium dumping indicated that three species were considered high-risk, seven are moderate-risk and five are low-risk (Tab.2).One important aspect is that most of the top 15 species display aggressive behavior (86.67%), a trait commonly associated with pet rejection among hobbyists and the consequent dumping into the new environments.

Discussion
We found a large number of species (n=93), most native to South America and traded among Brazilian hobbyists over the study period (almost five years), indicating that many ornamental non-native large fishes are available in the unregulated market.Our study is just a sample of the nonregulated market, so the number of new species and flow of fish among hobbyists must be much higher.For example, sales of largemouth bass Micropterus salmoides (Lacepède, 1802), Mexican mojarra Mayaheros urophthalmus (Günther, 1862) and Ginean bichir Polypterus ansorgii Boulenger, 1910, juveniles emerged in one of the monitored groups during March and April 2017 (A.L.B.Magalhães, pers.obs.), although these non-native species were not detected in our survey.In addition, we monitored only ten aquarium groups, but a quick search on Facebook ® showed the existence of at least 20 groups selling JNLF.Large-bodied species were formerly sold only in aquarium stores, but the popularity of social media and e-commerce increased the potential market.At present, JNLF can be easily purchased by consumers located outside large urban centers, a nonmonitored system that may enhance aquarium dumping and fish invasions across the country.
In our survey, Cichlidae was the main family in the informal market.Cichlids are among the most popular aquarium fishes due to aesthetic aspects such as diversity of colors (Mann, Sefc, 2013) and easiness of rearing in aquaria (Liang et al., 2006).Many hobbyists maintain their own breeding stocks, which also explains the desirability for this family (Liew et al., 2012).Several cichlids, however, are highly territorial, predatory and grow to large sizes, i.e, traits that make theses fishes good candidates to become undesirable and dumped.In the wild, large cichlids exhibit extended breeding seasons and aggressive parental care (Bomford, Glover, 2004), enhancing survival of the young and granting them competitive advantage over native species (van Breukelen, 2015).In addition, some nonnative species found here such as hybrid flowerhorn, oscar, banded cichlid and the lowland cichlid Herichthys carpintis are euryhaline, able to survive in mesohaline conditions for extended periods of time (Jaafar et al., 2012;Liew et al., 2012;Gutierre et al., 2016;Froese, Pauly, 2016), with the possibility to use brackish waters of mangroves/estuaries as dispersal routes (i.e, dispersion bridges) (Gutierre et al., 2014).Of the 11 cities evaluated, seven (63.64%) have mangroves and estuaries in their urban perimeters; if these euryhaline species invade these environments, the chance of establishment is high.
All species recorded were traded as juveniles at very small lengths, but all can attain large sizes at maturity; in addition, the majority display aggressive behavior.The same trend was found by Holmberg et al. (2015) for more than 700 large marine aquarium fish species, such as the giant grouper Epinephelus lanceolatus (Bloch, 1790) and the lionfish Pterois volitans (Linnaeus, 1758), sold in the U.S.A. aquarium trade.The small size at the retailing stage is a key factor behind the introduction of large-sized fishes, because many hobbyists are ignorant about species biology and behavior.Species biology may influence the likelihood of deliberate releases in two ways: first and most important, fish become too large and aggressive (Duggan et al., 2006;Gertzen et al., 2008); and second, proliphic species (e.g.some cichlids) may quickly overpopulate the aquaria, especially because fecundity is size-dependent (Liew et al., 2012).Both aspects are the main reasons for deliberate aquarium fish releases (Bomford, Glover, 2004;Magalhães, Jacobi, 2013a).
Tab. 2. Results of the Fish Invasiveness Screening Test (FIST) calculated for the 15 most available non-native large fishes.1: Maximum adult length (cm), 2: Aggressiveness, 3: Tolerance to salinity, 4: History of establishment, 5: Ability to breed in the wild, 6: Competition with native species, +: low; ++: moderate, +++: high.FD% = frequency of +++ among traits.Top eight JNLF commonly sold in Brazil have already invaded different regions of the planet, some with negative effects on biodiversity.For example, the hybrid flowerhorn is established in Sulawesi and threatens the endemic goby Glossogobius matanensis (Weber, 1913) through predation and competition (Herder et al., 2012).Astronotus ocellatus competes with native species in canals of the Everglades National Park, U.S.A (Trexler et al., 2000).Pangasianodon hypophthalmus introduced in Poland either hosts or transmitted a monogenoid parasite, Thaparocleidus caecus (Mizelle & Kritsky, 1969), posing threat to native fishes (Wiecaszek et al., 2009).A concerning trend is the increasing demand for peacock basses (Cichla) as pet fish.These fishes are the major group of piscivorous cichlids in South America, successful invaders of environments disturbed by human activities (Espínola et al., 2010).In Brazil, two large cichlids, C. piquiti and C. kelberi, are extensively established in non-Amazonian basins (Carvalho et al., 2014), and studies have shown that the introduction of these fishes is associated with deleterious effects on local fish assemblages (Carvalho et al., 2014;Pelicice et al., 2015).Although the invasion of Cichla is usually associated to sport fisheries, the importance of aquarium dumping may increase in next years, since these species are now popular among hobbyists in Brazil and elsewhere.We highlight that the Fish Invasiveness Screening Test has identified A. gigas, C. kelberi and C. temensis as high-risk species.As preventive measure, we recommend stringent control on the trade of giant arapaima and peacock basses.Top-predators have great potential to negatively affect the abundance of native biota and cause the extirpations of benthic invertebrates and fish (Gallardo et al., 2016).
The southeast region showed the greatest availability of JNLF especially in São Paulo and Rio de Janeiro.These cities, located in areas of Atlantic Rainforest, one of the world's biodiversity hotspots, are the most populous in the country.They are also the main center of aquarium trade, with more than 1,000 aquarium stores (Pinheiro et al., 2008) and thousands of fishkeepers (Magalhães, Jacobi, 2010).This geopolitical region has also the highest number of non-native large fishes introduced due to aquarium dumping, such as the goldfish C. auratus (Linnaeus, 1758), koi carp Cyprinus carpio Linnaeus, 1758, pike cichlid Crenicichla macrophthalma Heckel, 1840, eartheater cichlids Geophagus proximus (Castelnau, 1855), G. surinamensis (Bloch, 1791), pond loach Misgurnus anguillicaudatus (Cantor, 1842), A. ocellatus and jaguar guapote Parachromis managuensis (Günther, 1867) (Gomes et al., 2011;Vitule et al., 2014a;Latini et al., 2016).According to Magalhães (2015), identifying high-risk areas is necessary to devise management measures in geographic regions where invasions are more likely.The release of non-native large fishes into urban waters of Brazil has a recent history, but the scenario indicates that invasibility is high.Many ecosystems are disturbed by multiple human activities such as reservoirs, public ponds and urbanized mangroves/estuaries (Magalhães, Jacobi, 2013a;França et al., 2017;Pelicice et al., 2017).In adition, several regions in Brazil have a constant warm climate (Magalhães, Jacobi, 2013a;Latini et al., 2016;França et al., 2017), a scenario that may enhance the establishment of tropical non-native fishes.Therefore, the growing popularity of these fishes (Gomes et al., 2011;Magalhães, Jacobi, 2013a;Assis et al., 2014;Garcia et al., 2014;Magalhães, 2015;França et al., 2017), coupled with densely populated cities (IBGE, 2016), indicate that fish invasions and subsequent establishment will increase in next years.We highlight, however, that the successful invasion of some ornamental non-native large fishes does not necessarily demand a high propagule pressure.For instance, the establishment of C. auratus in Teller Lake #5, Colorado State (U.S.A), is believed to have stemmed from the release of a small number of founder fish, probably as unwanted pets.This species, with a current population of 3,000 to 4,000 individuals, is now a significant pest threatening local wildlife (Bryner, 2015).
Our findings suggest the need to improve management strategies to prevent further introductions of JNLF via aquarium dumping.Firstly, given that home aquariums are the major potential source of future invaders, a more rigorous system controlling fish keeping should be priority.Thus, we recommend authorities to advise and encourage hobbyists toward better practices concerning the correct disposal of nuisance fish.Aquarium stores and traders could teach hobbyists to return undesirable fishes to retailers (i.e, "reverse logistics") or donate to public institutions (e.g.schools, zoos).A more stringent and effective measures is euthanizing undesirable fishes (Gomes et al., 2011), although hobbyists usually show resistance.Secondly, environmental agencies should work together with Facebook ® Serviços Online do Brasil Ltda. to post alert messages in the pictures of JNLF for sale in aquarium groups, indicating simple ecological traits and other information (e.g.adult sizes, feeding behavior, tolerance to salinity, aggressiveness, prolificacy, disease vector).Recently, Magalhães, Jacobi (2010) suggested Brazilian virtual petshops and other social media to inform hobbyists about species traits as a means of reducing rejection and subsequent aquarium dumping.Thirdly, environmental agencies (e.g.Brazilian Institute of Environment and Renewable Natural Resources-IBAMA) must look for new communication tools, like the newly WhatsApp Messenger (www.whatsapp.com)or develop other smartphone apps, which provides an effective mean to reach hobbyists.For example, environmental agencies of U.S.A, Europe and the Fundación Humedales (Colombia) has developed free apps named respectively IveGot1, That's Invasive!and InvBasa, to provide awareness about new invasions (Adriaens et al., 2015;Wallace et al., 2016, Fundacion Humedales, 2017).Lastly, and more importantly, it is necessary to implement educational programs to provide high-quality information to hobbyists, retailers and fish farmers (Azevedo-Santos et al., 2015), as for example, informing about threats , Liew et al. (2012), Motionaquaticsuk (2016), Froese, Pauly (2016), Nelson et al. (2016), and Eschmeyer et al. (2017).