Escapes of non-native fish from flooded aquaculture facilities : the case of Paranapanema River , southern Brazil

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.

Freshwater aquaculture is strongly reliant on non-native fish species, which often become a problem when they escape (De Silva et al. 2009, Ortega et al. 2015, Davies and Britton 2016, Pelicice et al. 2017).Several fish species, including the tilapia, e.g.Oreochromis niloticus (Linnaeus, 1758), and the common carp, Cyprinus carpio Linnaeus, 1758, are cultured globally (Gozlan 2008).In fact more tilapia is produced in their invasive range than in their native African range (Gozlan et al. 2010).Non-native freshwater fish can escape into the basins, especially in facilities that provide no barriers to fish dispersal (Marchini et al. 2008, Ortega et al. 2015, Davies and Britton 2016).
In some countries, especially those with developing economies (e.g., Brazil, Peru, Colombia), priorities are often given to activities that generate revenues, irrespective of whether these could lead to environmental impacts (Gherardi et al. 2011, Pelicice et al. 2017).In Brazil, for example, whilst legislation is there to protect and limit the use of non-native species in freshwater aquaculture activities (Ayroza et al. 2006), there are public policies that encourage the use of non-native fishes that disregard the impacts these species could have in the neighbouring waterbodies (Lima Junior et al. 2012, Vitule et al. 2012, Orsi and Britton 2014, Pelicice et al. 2014, Casimiro et al. 2015, Lima et al. 2016, Padial et al. 2016, Pelicice et al. 2017).
The release of non-native fish from aquaculture sites occurs through a variety of mechanisms, including their direct stocking into natural systems (Agostinho et al. 2016), the escape of individual fish from open net-cages that are placed in reservoirs in intensive aquaculture systems (Agostinho et al. 2007, Azevedo-Santos et al. 2011), and escapes from ponds built in the margins of rivers that are inundated with water during floods (Orsi and Agostinho 1999).In Brazilian freshwater aquaculture, fish are frequently cultivated in production ponds located in river margins, with severe floods during the 1996/1997 El Niño resulting in approximately 1.29 million individuals belonging to 11 fish species and one hybrid being released from ponds into the Paranapanema River (Orsi and Agostinho 1999).These escapes were attributed to poor project planning, illegal aquaculture installations and/or farming facilities being inadequately installed in riparian areas prone to floods.Since then, aquaculture activities have increased in the basin in response to the development programs applied by the Brazilian Government (SEAB/DERAL 2016).
Since this major flood event in 1996/97, the risk of fish farms causing further releases of non-native fishes has actually increased due to the Brazilian Forest Code (Law 12,651/12) that reduces the Permanent Preservation Area (Casatti 2010, Magalhães et al. 2011, Forneck et al. 2016).The rainy season of 2015/16 was exceedingly wet in southern Brazil, also a consequence of El Niño rains, and resulted in extreme flooding in the Lower and Middle Paranapanema River basin and that resulted in number of fish farms being inundated with floodwater.The aim of this study was to therefore record the species richness and abundance of non-native fish that escaped during these flood events in 2015/16 to enable comparison with those that occurred in 1996/97.
Information on species richness and number of escaped fish was obtained from interviews conducted at aquaculture sites in the Lower and Middle Paranapanema River that could have been affected by the El Niño floods (Fig. 1).The total number of sites surveyed was 12, comprising eight sites that specialised in fish production (e.g., tilapias) and four sites that specialised in providing angling opportunities for paying anglers ('fish and pay' sites).At each site, structured interviews were used to gather data between April and August 2016 (i.e. in the post-flooding period).These interviews included the following questions: (i) What species are produced on the site?(ii) Were any hybrid forms produced and, if so, between which species? (iii) Were any fishes lost during the El Niño floods and, if so, how many of each species?and (iv) What was the area of production ponds affected (ha)?These data were analysed to determine the fishes being cultivated, the number of individuals that were dispersed into the river by the floods and the total area affected.The geographic locations of the sites were obtained via GPS (Garmin; 5 m accuracy).
The results of the interviews indicated that the number of escaped fish varied considerably between the 12 facilities, ranging between 500 and approximately 1,000,000 individuals, with a total estimate of approximately 1.14 million (M) juvenile and adult fishes released into the wild (Table 1).These fishes belonged to 21 species and three hybrid varieties (Table 1).The main species that escaped were the tilapias O. niloticus and Coptodon rendalli (Boulenger, 1897), with these comprising 96% of all escaped fishes.Among the 24 fish species released, 14 were non-native to the upper Paraná River basin, corresponding to 98% of all escapee fish.From the three hybrids detected (7,500 individuals), two had at least one parental non-native fish in the basin: tambacu (Piaractus mesopotamicus x Colossoma macropomum), and pintachara (Pseudoplatystoma corruscans x Pseudoplatystoma fasciatum), and one with no parental species native of the basin (jundiara, Leiarius marmoratus x Pseudoplatystoma reticulatum).Additionally, 400 individuals of two species were recorded as present in the Paranapanema River basin for the first time: pirarucu Arapaima gigas (Schinz, 1822) and pirarara Phractocephalus hemioliopterus (Bloch & Schneider, 1801) that, both escaped from 'fish and pay' angling.Comparison with data from the flood event in 1996/97 (Orsi and Agostinho 1999) revealed there was an increase in the number of species cultivated, with native species increasing from one to seven species, non-native species from nine to 14 species and hybrid fishes from one to three (Fig. 2).Despite the addition of native species cultivated, the number of individuals belonging to native species still comprised only 1% of all escaped fish in 2015/2016 (Table 1).
These data reveal that the flood events of 2015/16 in the Paranapanema River basin resulted in substantial numbers of non-native fish escaping from aquaculture sites along the river.A new event occurred almost 20 years after a previous flood event that caused a similar effect (Orsi and Agostinho 1999), and nothing was done to prevent further escapes.However, with the relaxation of legislation that previously protected forested riparian areas (Casatti 2010, Magalhães et al. 2011), coupled with increased recreational fishing activities ('fish and pay' facilities) (Fernandes et al. 2008), aquaculture parks (Lima et al. 2016) and the encouraging of the production of non-native species (Law 5989/09) (Pelicice et al. 2014, Casimiro et al. 2015), there was, by consequence, a repeat escape event.This also, indicates that biosecurity measures remained inadequate, allied with inspections by the relevant regulatory authorities not being sufficient to remedy this.
Compared with the study of Orsi and Agostinho (1999) on the 1996/97 flood event when 38 facilities were visited and interviewed, 12 were studied in 2015/16.Yet the estimated absolute number of escapee individual fish was similar (1.14 M versus 1.29 M), suggesting increases in the number of fish produced per facility (Flores and Pedroza-Filho 2014, Forneck et al. 2016, SEAB/DERAL 2016).Massive escapes suggest that the recent modifications in the Brazilian Forest Code that have relaxed controls on the culture around the river has resulted in a substantial risk of spreading cultivated fishes into the wild (Magalhães et al. 2011).
Even the introduction of native species from aquaculture can present risk to wild populations, such as by reducing genetic variability in the population into which they are released (Pereira et al. 2010).Aquaculture may inadvertently decrease the genetic variability present in farmed stocks by the selection and breeding of related specimens or by the use of a small number of parents as brood stock (Kostow 2009, Almeida et al. 2013).The introduction risk is compounded by a range of additional consequences that non-native fishes can have in the wild, including altered habitat structure, hybridization, disease transmission, and increased trophic interactions (e.g.predation and competition) that can lead all negatively impact native fauna (Agostinho et al. 2007, Vitule et al. 2009, Ashikaga et al. 2010, Alves et al. 2014).
The decreased controls of the production of non-native fish species in Paranapanema River basin over the last twenty years have also been concomitant with an increase in the number of 'fish and pay' sites.These are fisheries used for angling that are mainly stocked with large-bodied fishes to maximise angler attraction and satisfaction, with species used including A. gigas, P. hemioliopterus, P. fasciatum, and Colossoma macropo-   In summary, the escapes of non-native and native fish from aquaculture and fishery activities in the Paranapanema River basin that occurred due to flooding during El Niño rains represent a high propagule pressure in a basin that is already invaded by a number of non-native fishes (Britton and Orsi 2012).If these unscheduled releases can be prevented in future, then environmental control agencies such as Brazilian Institute of Environment Renewable Natural Resources (IBAMA) should work together with aquaculturists, fry producers, aquaculture associations, 'fish and pay' owners, and conservationists to find optimal solutions.Solutions could include: (i) application of the precautionary principle or 'polluter pays' principle to minimise the risk of escapee fish entering the wider environment; (ii) increase of pond embankment height to prevent escape of the species during periods of flooding; and (iii) construction of containment structures that provide some biosecurity during inundation events.These recommendations would help Brazilian government to meet its international commitments in controlling non-native species whilst ensuring aquaculture can continue high rates of fish production and maintain food supplies without losing their stock during flood events.With the increase of aquaculture in Brazil, if these protection recommendations are not considered, new escapes of non-native fishes into the basin are likely to be a re-occurring issue, especially during future flood events.

Figure 1 .
Figure 1.Map of the Paranapanema River basin with the location of the evaluated areas (red dots: fish production, blue dots: 'fish and pay').

Figure 2 .
Figure 2. Number of fish species escaped (native, non-native and hybrid) in the Lower and Middle Paranapanema River basin during the floods of 1996/1997 (Orsi and Agostinho 1999) and 2015/2016.

Table 1 .
Escapes of non-native fish from flooded aquaculture facilities Absolute (relative) abundance and origin of fish species and hybrids registered in the escapes from fish ponds of the Paranapanema River basin during the flood of 2015/2016.Classification and origin are based on Eschmeyer (2017).*Non-native species, **unquantified species.