Range expansion of Procambarus clarkii (Girard, 1852) (Decapoda: Cambaridae) in southern Brazil

Abstract

The crayfish Procambarus clarkii (Girard, 1852) is a native species from the south-central region of the USA and northeastern Mexico that has been introduced to all continents except Antarctica and Oceania. In Brazil, P. clarkii has 17 established populations, all found in the southeastern region. The studied specimens were obtained at Ribeirão Claro municipality (23°11’38”S 49°45’28”W) in Paraná State, southern Brazil, in fish ponds from a private property near the Paranapanema River reservoir. Sampling was performed in September 2013 and March 2015, yielding a total of 13 crayfish specimens. Interviews with residents and workers at the sampling sites revealed that the aquarium trade could be an important introductory pathway, since the first crayfish observed had been released into nature shortly after being purchased at a pet shop in the neighboring state of São Paulo; even though current legislation forbids their importation, transportation, and commercialization.

Keywords
Alien biology; ecological plasticity; exotic crayfish; illegal; species expansion

The red swamp crayfish Procambarus clarkii (Girard, 1852) is native to south-central USA (Louisiana) and northeastern Mexico (Hobbs and Jass, 1989). This species shows ecological plasticity, being able to thrive in harsh environments (Dörr et al., 2006) because of its high reproductive output and brief developmental period, and ability to modify its feeding habits (Anastácio et al., 2014). The red swamp crayfish is a widespread invasive species (Magalhães et al., 2005; Chucholl, 2011; Loureiro et al., 2015) that can be found on all continents except Australia and Antarctica (Hernández et al., 2008; Loureiro et al., 2015). It has commercial value as a food source and as pets in the aquarium trade (Magalhães et al., 2005; Loureiro et al., 2015). However, the commercialization of this species may ultimately harm aquatic habitats and the organisms dependent on these habitats (Usio and Townsend, 2004), including native populations of crayfish, fish, amphibians, and macroinvertebrates (Rodríguez et al., 2005).

Since 1985, 17 established populations of P. clarkii have been recorded in Brazil, all located in the southeast region of São Paulo State (Magalhães et al., 2005; Loureiro et al., 2015). The specimens were introduced either accidentally or deliberately via the aquarium trade (Loureiro et al., 2015). The aim of this study is to present the first record of this species in Paraná State, southern Brazil, expanding its range of invasion in the country.

The specimens of P. clarkii were sampled in Ribeirão Claro (23°11’38”S 49°45’ 28”W) in Paraná State, south of Brazil, in a fishpond from a private property near the Paranapanema River reservoir (Fig. 1). Samplings were performed in September 2013 and March 2015, and all animals were captured with a hand-net and individually placed in bags to ensure morphological integrity.

Figure 1.
Map showing records of Procambarus clarkii (Girard, 1852) in Brazil. White circles indicate previous records from Magalhães et al. (2005) and Loureiro et al. (2015). White triangle represents the present record.

In the laboratory, the crayfish were identified using Hobbs (1974). Each specimen had its carapace length (CL) measured with a caliper (0.01-mm specificity). Ten specimens were stored in 70% ethanol and deposited in the Scientific Collection of the Study Group on Crustacean Biology, Ecology and Culture from the Institute of Biosciences of Botucatu, São Paulo State University (Nebecc - IBB - Unesp). Three selected specimens were fixed in 70% ethanol (one male morphotype I, one male morphotype II, and one female) and deposited in the Carcinological Collection of the Museum of Zoology of the University of São Paulo (MZUSP #36845).

Thirteen crayfish were sampled, five of which were male [one morphotype I and four morphotype II] (Fig. 2D-F) and eight of which were female. Thirteen specimens were examined, ten in September 2013 and three in March 2015, revealing a mean CL size of 26.9 ± 4.9 mm (MZUSP #36845; collector: M. Antunes). Respondents who live and work in the sampling region reported that one crayfish was purchased in a pet store in São Paulo State to be kept as a pet in January 2013. After a couple of days, the specimen was released into the fishpond and local workers and fishermen began to notice the permanence of P. clarkii on site. The crayfish were observed walking along the fish ponds, and even managed to damage one of the ponds due to its burrowing behavior (Fig. 2A-C).

Figure 2.
Sampling sites: A-C. Procambarus clarkii (Girard, 1852) individuals, morphotype I male (reproductive form): D-F, lateral, dorsal, and ventral views, respectively. Images by: Antunes, M.

Our study presents a new southernmost record for P. clarkii in Brazil (Paraná State). The authors offer a possible dispersion pathway, namely, active dispersal through water bodies that connect hydrographic basins (i.e., rivers and ponds). Additionally, P. clarkii is easily available for sale in the pet and aquarium trades (Magalhães et al., 2005; Loureiro et al., 2015) even though the current legislation forbids its importation, transportation, and commercialization (IBAMA, 2008).

Since both male morphotypes were sampled, we can assume that the population is established and reproducing on-site. Once the population of P. clarkii is established, it can damage local fauna and flora (Rodríguez et al., 2005). The red swamp crayfish is an effective grazer and can destroy aquatic macrophytes, initiating a cascade of detrimental events on the entire local fauna, since fishes, amphibians, and some macroinvertebrates use macrophytes as a refuge for their larvae (Rodríguez et al., 2005). This crayfish exhibits burrow-construction behavior that can be used to manipulate its environment, thus altering sediment characteristics, impoverishing water quality, and increasing turbidity (Huner and Barr, 1991; Angeler et al., 2001; Barbaresi and Gherardi, 2006). Possible contact between P. clarkii and other endemic crayfish is viewed as a major threat to the native crayfish, mainly because of the possibility of Aphanomyces astaci, a fungal-like organism (Oomycete), transmission. The pathogen chronically infects North American endemic crayfish, such as P. clarkii (see Peiró et al., 2016).

Twelve species of native Brazilian crayfish are currently described, of which eight are endemic, belonging to the genus Parastacus Huxley, 1879 and restricted to southern Brazil, i.e., Santa Catarina and Rio Grande do Sul States (Ribeiro et al., 2016; 2017; Huber et al., 2018; Miranda et al., 2018; Ribeiro et al., 2020). Another group that could be threatened by the red swamp crayfish is the Aeglidae, a group of freshwater anomurans native to southern South America, with many endemic species (Pérez-Losada et al., 2009). Currently, there are 55 species of Aegla distributed in Brazilian basins (Páez et al., 2018; Trombetta et al., 2019) with many species vulnerable and already endangered (Moraes et al., 2017).

If P. clarkii continues to spread further south, it could soon threaten native Brazilian decapod species, since invasive crayfish are known to dominate native crayfish when fighting for a resource, securing the resource for longer and behaving more aggressively (Dalosto et al., 2015). The Parastacidae inhabiting Brazilian territory are often located in hydrographic basins that connect to Argentina and Uruguay (Ribeiro et al., 2020). Thus, this scenario poses a risk to endemic parastacids if red swamp crayfish invade other countries in South America, as predicted by Palaoro et al. (2013).

The original collection ponds were revisited three years later, and the locals reported a decrease in the sightings of P. clarkii. The amount of crayfish caught in fishnets also decreased due to the farming of fish belonging to the genera Serrasalmus Lacepède, 1803 and Hoplias Gill, 1903 for sport-fishing purposes. Later, in 2018, the local fishermen and residents reported only carapace traces along the pond margins. It is important to observe that these cultivated fish species [Serrasalmus marginatus Valenciennes, 1837, Serrasalmus maculatus Kner, 1858 and Hoplias malabaricus (Bloch, 1794)] occur naturally in the region (Duke Energy, 2008). The introduction of these predatory fish is an effective tool in crayfish management, representing an intense predation pressure that may be an effective alternative for extensive capture that yielded, according to Loureiro et al. (2018), no satisfactory results.

Given these considerations, Brazilian laws regulating the commerce of P. clarkii should be enacted and enforced, and regions with P. clarkii populations should be regularly monitored due to the imminent risk of invasion of this species further south. This invasion could potentially threaten native Brazilian crayfish and aeglids, which are less aggressive than the invasive crayfish and display high levels of endemism, thus, with a potential to cause irreversible damage. Furthermore, the pond sampled is close to the Paranapanema River basin, which includes several lotic systems that could be a potential invasion pathway. Lotic systems may accelerate invasion processes, as recorded in northern Brazil where Macrobrachium rosenbergii (De Man, 1879) co-occurs with native species (Silva-Oliveira et al., 2011; Iketani et al., 2016). Therefore, continuous monitoring of the status of the P. clarkii and its potential effects on the biodiversity of the basin is of great importance in order to impose actions to avoid damage to local biological communities.

ACKNOWLEDGEMENTS

We are grateful to Amaury Antunes and João Marques for their support during field activities and to Bruno Siqueroli for allowing us to sample P. clarkii specimens on his farm and for sharing his observations on crayfish from Ribeirão Claro, Paraná State, Brazil. We also thank Dr. Daniel Marcondes Lima for helping with the museum deposit process and Ms. Julia Fernandes Perroca for assisting with the map.

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Publication Dates

• Publication in this collection
  28 Oct 2020
• Date of issue
  2020

History

• Received
  20 Jan 2020
• Accepted
  08 July 2020