ZOOLOGIA 35: e14638 ISSN 1984-4689 (online) zoologia.pensoft.net SHORT COMMUNICATION Escapes of non-native fish from flooded aquaculture facilities: the case of Paranapanema River, southern Brazil Armando César Rodrigues Casimiro1, Diego Azevedo Zoccal Garcia1, Ana Paula Vidotto-Magnoni1, John Robert Britton2, Ângelo Antônio Agostinho3, Fernanda Simões de Almeida4, Mário Luís Orsi1 1Laboratório de Ecologia de Peixes e Invasões Biológicas, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina. 86057-970 Londrina, PR, Brazil. 2Centre for Conservation Ecology and Environmental Sciences, School of Applied Sciences, Bournemouth University. Poole, BH12 5BB, United Kingdom. 3Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Departamento de Biologia, Universidade Estadual de Maringá. 87020-900 Maringá, PR, Brazil. 4Laboratório de Genética e Ecologia Animal, Departamento de Biologia Animal e Vegetal, Universidade Estadual de Londrina. 86057-970 Londrina, PR, Brazil. Corresponding author: Armando César Rodrigues Casimiro ([email protected]) http://zoobank.org/6EE0B6B2-8319-4766-94CE-6C4233CE96DC ABSTRACT. Non-native species are a major driver of biodiversity loss. Aquaculture activities play a key role in introductions, including the escape of fishes from fish farm facilities. Here, the impact of flooding due to El Niño rains in 2015/2016 in the Lower and Middle Paranapanema River basin, southern Brazil, was investigated by evaluating fish escapes from 12 fish farms. The flooding resulted in the escape of approximately 1.14 million fishes into the river, encompassing 21 species and three hybrids. Non-native species were the most abundant escapees, especially Oreochromis niloticus (Linnaeus, 1758) and Coptodon rendalli (Boulenger, 1897) (96% of all fish). Only seven native fishes were in the escapee fauna, comprising 1% of all fish. Large floods, coupled with inadequate biosecurity, thus resulted in considerable inputs of non-native fish into this already invaded system. KEY WORDS. Biological invasion, climate change, fish farming, Paraná River, propagule pressure. Freshwater aquaculture is strongly reliant on non-native Pelicice et al. 2017). In Brazil, for example, whilst legislation fish species, which often become a problem when they escape is there to protect and limit the use of non-native species in (De Silva et al. 2009, Ortega et al. 2015, Davies and Britton 2016, freshwater aquaculture activities (Ayroza et al. 2006), there are Pelicice et al. 2017). Several fish species, including the tilapia, public policies that encourage the use of non-native fishes that e.g. Oreochromis niloticus (Linnaeus, 1758), and the common disregard the impacts these species could have in the neighbour- carp, Cyprinus carpio Linnaeus, 1758, are cultured globally (Go- ing waterbodies (Lima Junior et al. 2012, Vitule et al. 2012, Orsi zlan 2008). In fact more tilapia is produced in their invasive and Britton 2014, Pelicice et al. 2014, Casimiro et al. 2015, Lima range than in their native African range (Gozlan et al. 2010). et al. 2016, Padial et al. 2016, Pelicice et al. 2017). Non-native freshwater fish can escape into the basins, especially The release of non-native fish from aquaculture sites in facilities that provide no barriers to fish dispersal (Marchini et occurs through a variety of mechanisms, including their direct al. 2008, Ortega et al. 2015, Davies and Britton 2016). stocking into natural systems (Agostinho et al. 2016), the escape In some countries, especially those with developing econ- of individual fish from open net-cages that are placed in reser- omies (e.g., Brazil, Peru, Colombia), priorities are often given to voirs in intensive aquaculture systems (Agostinho et al. 2007, activities that generate revenues, irrespective of whether these Azevedo-Santos et al. 2011), and escapes from ponds built in the could lead to environmental impacts (Gherardi et al. 2011, margins of rivers that are inundated with water during floods ZOOLOGIA 35: e14638 | DOI: 10.3897/zoologia.35.e14638 | May 23, 2018 1 / 6 A.C.R. Casimiro et al. (Orsi and Agostinho 1999). In Brazilian freshwater aquaculture, non-native to the upper Paraná River basin, corresponding to fish are frequently cultivated in production ponds located in 98% of all escapee fish. From the three hybrids detected (7,500 river margins, with severe floods during the 1996/1997 El Niño individuals), two had at least one parental non-native fish in resulting in approximately 1.29 million individuals belonging the basin: tambacu (Piaractus mesopotamicus x Colossoma macro- to 11 fish species and one hybrid being released from ponds pomum), and pintachara (Pseudoplatystoma corruscans x Pseudo- into the Paranapanema River (Orsi and Agostinho 1999). platystoma fasciatum), and one with no parental species native These escapes were attributed to poor project planning, illegal of the basin (jundiara, Leiarius marmoratus x Pseudoplatystoma aquaculture installations and/or farming facilities being inade- reticulatum). Additionally, 400 individuals of two species were quately installed in riparian areas prone to floods. Since then, recorded as present in the Paranapanema River basin for the aquaculture activities have increased in the basin in response to first time: pirarucu Arapaima gigas (Schinz, 1822) and pirarara the development programs applied by the Brazilian Government Phractocephalus hemioliopterus (Bloch & Schneider, 1801) that, (SEAB/DERAL 2016). both escaped from ‘fish and pay’ angling. Comparison with Since this major flood event in 1996/97, the risk of fish data from the flood event in 1996/97 (Orsi and Agostinho farms causing further releases of non-native fishes has actually 1999) revealed there was an increase in the number of species increased due to the Brazilian Forest Code (Law 12,651/12) cultivated, with native species increasing from one to seven that reduces the Permanent Preservation Area (Casatti 2010, species, non-native species from nine to 14 species and hybrid Magalhães et al. 2011, Forneck et al. 2016). The rainy season of fishes from one to three (Fig. 2). Despite the addition of native 2015/16 was exceedingly wet in southern Brazil, also a conse- species cultivated, the number of individuals belonging to quence of El Niño rains, and resulted in extreme flooding in the native species still comprised only 1% of all escaped fish in Lower and Middle Paranapanema River basin and that resulted 2015/2016 (Table 1). in number of fish farms being inundated with floodwater. The These data reveal that the flood events of 2015/16 in the aim of this study was to therefore record the species richness Paranapanema River basin resulted in substantial numbers of and abundance of non-native fish that escaped during these non-native fish escaping from aquaculture sites along the river. flood events in 2015/16 to enable comparison with those that A new event occurred almost 20 years after a previous flood occurred in 1996/97. event that caused a similar effect (Orsi and Agostinho 1999), Information on species richness and number of escaped and nothing was done to prevent further escapes. However, with fish was obtained from interviews conducted at aquaculture sites the relaxation of legislation that previously protected forested in the Lower and Middle Paranapanema River that could have riparian areas (Casatti 2010, Magalhães et al. 2011), coupled with been affected by the El Niño floods (Fig. 1). The total number increased recreational fishing activities (‘fish and pay’ facilities) of sites surveyed was 12, comprising eight sites that specialised (Fernandes et al. 2008), aquaculture parks (Lima et al. 2016) and in fish production (e.g., tilapias) and four sites that specialised the encouraging of the production of non-native species (Law in providing angling opportunities for paying anglers (‘fish and 5989/09) (Pelicice et al. 2014, Casimiro et al. 2015), there was, pay’ sites). At each site, structured interviews were used to gather by consequence, a repeat escape event. This also, indicates that data between April and August 2016 (i.e. in the post-flooding biosecurity measures remained inadequate, allied with inspec- period). These interviews included the following questions: (i) tions by the relevant regulatory authorities not being sufficient What species are produced on the site? (ii) Were any hybrid to remedy this. forms produced and, if so, between which species? (iii) Were Compared with the study of Orsi and Agostinho (1999) any fishes lost during the El Niño floods and, if so, how many on the 1996/97 flood event when 38 facilities were visited and of each species? and (iv) What was the area of production ponds interviewed, 12 were studied in 2015/16. Yet the estimated affected (ha)? These data were analysed to determine the fishes absolute number of escapee individual fish was similar (1.14 being cultivated, the number of individuals that were dispersed M versus 1.29 M), suggesting increases in the number of fish into the river by the floods and the total area affected. The ge- produced per facility (Flores and Pedroza-Filho 2014, Forneck ographic locations of the sites were obtained via GPS (Garmin; et al. 2016, SEAB/DERAL 2016). Massive escapes suggest that 5 m accuracy). the recent modifications in the Brazilian Forest Code that have The results of the interviews indicated that the number relaxed controls on the culture around the river has resulted of escaped fish varied considerably between the 12 facilities, in a substantial