BioInvasions Records (2020) Volume 9, Issue 2: 357–366

CORRECTED PROOF

Research Article Establishment of the exotic invasive redclaw quadricarinatus (Von Martens, 1868) in the Coastal Plain of San Blas, Nayarit, SE Gulf of California, Mexico

José R. Tapia-Varela1, Jesús T. Ponce-Palafox1,2,*, Deivis S. Palacios-Salgado2,†, Carlos A. Romero-Bañuelos1, José T. Nieto-Navarro2 and Pedro Aguiar-García3 1Secretaría de Investigación y Posgrado, Universidad Autónoma de Nayarit, Tepic, Nayarit 63000, México 2Escuela Nacional de Ingeniería Pesquera, Universidad Autónoma de Nayarit, Bahía de Matanchén, San Blas, Nayarit 63740, México 3Unidad Académica de Medicina. Universidad Autónoma de Nayarit. Tepic, Nayarit 63000, México Author e-mails: [email protected] (JRTV), [email protected] (JTPP), [email protected] (DSPS), [email protected] (CARB), [email protected] (JTNN), [email protected] (PAG) *Corresponding author

Citation: Tapia-Varela JR, Ponce-Palafox JT, Palacios-Salgado DS, Romero- Abstract Bañuelos CA, Nieto-Navarro JT, Aguiar- García P (2020) Establishment of the The establishment of the redclaw crayfish () populations was exotic invasive redclaw crayfish Cherax investigated in the coastal plain of San Blas, Nayarit State, Mexico. Two sampling quadricarinatus (Von Martens, 1868) in expeditions were conducted along the agricultural irrigation channels and the the Coastal Plain of San Blas, Nayarit, SE surrounding estuarine systems in the study area in December 2014 and December Gulf of California, Mexico. BioInvasions Records 9(2): 357–366, https://doi.org/10. 2015. A total of 121 specimens were collected during the first sampling. They had 3391/bir.2020.9.2.21 1:1.88 male:female ratio. Three hundred fourteen (314) individuals were collected in the second expedition, the male:female ratio was 1:1.27. C. quadricarinatus has Received: 29 November 2019 a great ability to colonize, invade and survive a wide range of environmental conditions Accepted: 10 February 2020 in aquatic ecosystems, representing a threat to biological diversity. This species has Published: 30 March 2020 the potential to replace the native crayfish species that significantly sustain the local Handling editor: David Hudson fisheries, affecting and limiting their distribution and abundance. This has probably Thematic editor: Vadim E. Panov affected diversity, population structure and symbiotic relationships of functional Copyright: © Tapia-Varela et al. groups in this aquatic ecosystem. This is an open access article distributed under terms of the Creative Commons Attribution License Key words: non-native species, freshwater, Río Grande de Santiago, invasion (Attribution 4.0 International - CC BY 4.0). OPEN ACCESS. Introduction Currently, Cherax quadricarinatus (Von Martens, 1868) is widely distributed in riverbeds, freshwater irrigation channels, and brackish-water lagoons and is a fast-growing species, reaching 250 mm total body length and 600 g average wet mass in 9 months (Ponce-Palafox et al. 1999, 2009; Belle et al. 2010). This crayfish has gregarious habits, flexible diet and high tolerance to physicochemical variations in the environment (Snovsky and Galil 2011). Also, it can tolerate a wide range of temperatures (7.8 to 38.0 °C) and salinities up to 8‰ (Ponce-Palafox et al. 2009). When the concentration of dissolved oxygen falls below 1 mg/L, C. quadricarinatus usually reaches the edge of aquatic systems where the oxygen level is optimal, and in extreme cases, it migrates out of the aquatic bodies (Mendoza-Alfaro et al.

Tapia-Varela et al. (2020), BioInvasions Records 9(2): 357–366, https://doi.org/10.3391/bir.2020.9.2.21 357 Establishment of Cherax quadricarinatus in the Coastal Plain of San Blas

2011). Hence, C. quadricarinatus is a species with the ability to colonize, invade, and survive a wide range of environmental conditions in aquatic ecosystems (Aguirre and Mendoza 2009). Studies in natural lentic and lotic environments with C. quadricarinatus have shown that this species can cause changes in littoral habitat, compete for refuge and food, and in some cases displace native species of fish (Poecilia reticulata) and freshwater prawns (Macrobrachium tenellum, M. americanum) (Ahyong and Yeo 2007; Vega-Villasante et al. 2015; Marufu et al. 2017, 2018; Petersen et al. 2017; Zeng et al. 2019). The redclaw crayfish Cherax quadricarinatus, is native to Australasia but is globally distributed because it is hatchery-reared and used for aquarium trade. Due to their escape from aquatic facilities, this species has become successfully established in different aquatic ecosystems as alien populations in Europe, Asia, America and Africa (Petersen et al. 2017). Cherax quadricarinatus populations have been introduced in the aquatic ecosystems of Latin America as is the case of Ecuador, Argentina, , Puerto Rico, Cuba, Mexico and others (Romero 1997; Ponce-Palafox et al. 1999, 2009; Vigliano and Darrigran 2002). The first attempt made to rear the redclaw crayfish in a hatchery in Mexico was in the State of Queretaro in 1986 and later, during 1995 in Mexico City (Ponce-Palafox et al. 1999; Rodríguez-Almaráz and García- Madrigal 2014). Since then, it has been raised in aquaculture facilities in several locations of México and due to this proliferation, an unknown number of escape events have occurred that led to the establishment of successful wild populations (Ponce-Palafox et al. 2009). In general, this species has been raised in aquaculture facilities in Aguascalientes, Baja California Sur, Chihuahua, Ciudad de México, Colima, Jalisco, Michoacán, Morelos, Nuevo León, Oaxaca, Puebla, Sinaloa, Tamaulipas, Veracruz and Yucatan states (Mendoza-Alfaro et al. 2011). Several studies have reported wild specimens in Tamaulipas, Nuevo León, Morelos, Jalisco, Sinaloa and San Luis Potosí states (Bortolini et al. 2007; Hernández et al. 2007; Ponce-Palafox et al. 2009; Rodríguez-Almaráz and García-Madrigal 2014; Vega-Villasante et al. 2015; Torres-Montoya et al. 2016; Rodríguez-Almaráz et al. 2018). In San Blas, Nayarit, the first exotic populations of C. quadricarinatus probably came from the state of Tamaulipas from where organisms were introduced for aquaculture purposes at an aquatic farm located in the town of Tizate (21°47′35.89″N; 105°06′38.30″W), Municipality of Santiago Ixcuintla, Nayarit, Mexico, in 2001. There were three introductions later, the first in a fish farm located three kilometers downstream of the first introduction, another close to Huaristemba town in a fish farm, and the last in a juvenile laboratory of Cherax near the town of Santa Cruz de Miramar. In this study, the first records of wild populations of C. quadricarinatus established in the central coastal plain of Nayarit State, Mexico are presented.

Tapia-Varela et al. (2020), BioInvasions Records 9(2): 357–366, https://doi.org/10.3391/bir.2020.9.2.21 358 Establishment of Cherax quadricarinatus in the Coastal Plain of San Blas

Figure 1. Sampling sites of Cherax quadricarinatus in low basin of Santiago River and Nayarit State, Mexico. Circles = sampling sites; Triangles = introduction sites

Materials and methods Study area The study area (21°39′41.12″N; 105°12′14.72″W) is located to the southeast of the low basin of the Río Grande de Santiago and part of the Huicicila- San Blas sub-basin in the State of Nayarit, Mexico (INEGI 1995). In these hydrological systems, there is a complex network of streams and artificial canals (Figure 1). Periodic flooding in the region is common especially during the rainy season with the Santiago River avenues where surplus water is present. The study area has a sub-humid climate, an average annual temperature greater than 22 °C and a minimum temperature of the coldest month of 18 °C. Precipitation during the dry season is less than 60 mm, and it has summer rains with precipitation/temperature (P/T) index between 43.2% and 55.3% and the percentage of winter rains from 5% to 10.2% of the total year (García 2004). The natural riverbeds, freshwater irrigation channels, and brackish water lagoons provide feasible conditions for fishing several commercial species such as Oreochromis spp., Centropomus spp., Lutjanus spp., Penaeus vannamei, Macrobrachium tenellum, M. digueti and M. americanum; the latter being the most valuable species in the local market.

Sampling sites Twenty-one (21) sampling sites at different locations, irrigation canals and water bodies in the study area were inspected between December 2014 and December 2015. The organisms were sampled in October, November and

Tapia-Varela et al. (2020), BioInvasions Records 9(2): 357–366, https://doi.org/10.3391/bir.2020.9.2.21 359 Establishment of Cherax quadricarinatus in the Coastal Plain of San Blas

Figure 2. Dorsal view of a male and female redclaw crayfish (C. quadricarinatus) found in the Coastal Plain of San Blas, Nayarit, SE Gulf of California, Mexico. Photo by JRTV.

December 2014 and 2015. One sample per month (3 samples per site) (Figure 1). The sampled sites were chosen base on the reports of farmers, agriculture and conservation officials on the existence of C. quadricarinatus. Alongside these hydrological systems, there is a large number of irrigation channels, reservoirs, and wetlands. In 2014 and 2015 began the sampling of “La Amapita” and “Toño Tapia” channels, surrounding Reforma Agraria Locality, Nayarit, Mexico (21°39′41.12″N; 105°12′14.72″W). Overall, the sampled sites were mainly in lotic habitats and having at least a space of 100 m to 2.0 km from each other. This depends on access to the waterways and water bodies.

Sampling procedure Sampling at each locality was done at night. There was an initial 10-minute observation of the sampling sites to locate the organisms or molts of the specimens being studied. The organisms were collected with a cast net (atarrayas) and traps using coconut pieces as attractants. In addition, four fishing traps were left overnight from 6:00 p.m. to 6:00 a.m. at each sampling site. In the water bodies, C. quadricarinatus sampling was done by a boat trip and making sets with cast net. Gravid females were collected and their reproductive capacity was estimated in terms of the number of eggs per gram of body mass (5.5 eggs/g). Each specimen was measured for total length with Vernier calipers (cm) by measuring the distance from the tip of the rostrum to the extreme of the telson. The masses of the organisms were determined with a digital field balance (OHAUS) and thereafter they were sexed (Figure 2).

Tapia-Varela et al. (2020), BioInvasions Records 9(2): 357–366, https://doi.org/10.3391/bir.2020.9.2.21 360 Establishment of Cherax quadricarinatus in the Coastal Plain of San Blas

Figure 3. Fishing gear used to capture Cherax quadricarinatus in Reforma Agraria, San Blas, Nayarit, Mexico: bucket traps (a), bucket traps uncovered (b), bucket traps outline (c) and nylon cast nets (d). Photo composition by authors JRTV, JTNN and JTPP.

Cherax quadricarinatus were collected in irrigation channels. The trap system varied from simple traps made with modified plastic buckets to nylon sweep nets with 12.7 mm mesh size (Figure 3). The redclaw crayfish captured were identified based on the morphological characters described by Souty-Grosset et al. (2006) and up to 13 g organisms were considered juveniles (Ponce-Palafox et al. 2009).

Statistical analysis Data were processed in Excel Software worksheets. Descriptive statistics such as mean, standard deviation and range were used to compare data between sampling expeditions. The length and mass data were checked using Levene’s test for homogeneity of variances and Shapiro-Wilk’s test for normality. To determine the differences in length and mass of females and males across four levels (2014 female, 2015 female, 2014 male, and 2015 male), one-way analysis of variance (ANOVA) was performed. Later Tukey’s test was used to determine which treatments differed significantly and Chi-square goodness-of-fit test was used assuming 1:1 ratio as the expected values between counts of male and female (Sokal and Rohlf 2013).

Results Cherax quadricarinatus was detected in all the 21 sites sampled in the coastal plain of the municipality of San Blas (Figure 1) during the two years of study (2014 to 2015), up to a distance of 37 km downstream from its

Tapia-Varela et al. (2020), BioInvasions Records 9(2): 357–366, https://doi.org/10.3391/bir.2020.9.2.21 361 Establishment of Cherax quadricarinatus in the Coastal Plain of San Blas

Table 1. Length and mass of Cherax quadricarinatus collected at the left margin of the low basin of Santiago River and Nayarit State, Mexico. Female Male Female Male Parameters/Sex 2014 2015 2014 2015 Mean total length (cm) 12.85 ± 1.61b 12.55 ± 2.36b 13.85 ± 1.55a 13.71 ± 2.64a Total length range (cm) 9.0–17.3 6.6–18.0 11.5–18.0 6.5–19.0 Mean mass (g) 54.05 ± 20.45b 40.69 ± 22.75b 59.62 ± 23.55a 60.66 ± 36.48a Mass range (g) 16.0–130.0 4.0–132.6 32.0–136.0 4.0–136.0 No. of organisms 79 176 42 138 Different upper letters in each row denote statistical significance (P < 0.05).

Table 2. Reproductive parameters and number of juveniles of Cherax quadricarinatus collected at the left margin of the low basin of Santiago River and Nayarit State, Mexico. Parameters/Year 2014 2015 No. of ovigerous females 2 4 Number of eggs per female 297 223 Sex ratio (M:F) 1:1.6a 1:1.3a No. of juveniles 4 6 Different superscript letters in each row denote statistical significance (P < 0.05)

introduction, indicating a spread rate of 2.2 km/year. The environments where C. quadricarinatus was found were streams, irrigation canals, water bodies and estuaries of low salinity. A total of 121 specimens were collected during the first sampling expedition, consisting of 42 males and 79 females (Table 1). During the second sampling expedition, 314 C. quadricarinatus specimens were collected, consisting of 138 males and 174 females (Table 1). The length and mass of the males collected were significantly (P < 0.05) higher than that of the females in the study periods and no significant (P > 0.05) intra-sexual differences were recorded during the study. The sizes obtained in the two years of sampling represent redclaw crayfish from juvenile to adult stages. There was tendency to capture higher mass organisms in December 2015. The maximum mass of each organism captured was 136 g in the same year. Ovigerous females were obtained from the sampling of 2014 and 2015 (Table 2). They were identified until stage 12 postembryonic II of egg development in which the development of the rostrum and ocular peduncle was shown as described by García-Guerrero et al. (2003). In the dry season, the sex ratio was significantly different from 1:1 (X2 = 3.942, p = 0.037). The studied materials from different locations were deposited in the Collection (CC-120) of Escuela Nacional de Ingeniería Pesquera from Universidad Autónoma de Nayarit, Mexico.

Discussion Cherax quadricarinatus collected in this study had a length of 6.5 to 19.0 cm greater than those obtained in Morelos (1.1 to 16.1 cm), Tamaulipas (3.2 to 16 cm) and Jalisco (9.6 to 11.7 cm) states in wild conditions (Bortolini et al. 2007; Vega-Villasante et al. 2015). The sex ratio was significantly different

Tapia-Varela et al. (2020), BioInvasions Records 9(2): 357–366, https://doi.org/10.3391/bir.2020.9.2.21 362 Establishment of Cherax quadricarinatus in the Coastal Plain of San Blas

from the expected 1:1 ratio as reported in other wild populations, especially in the dry season. However, it is required to determine sampled site effects of gender, length, and mass at the larger-scale of the coastal plain of San Blas. No C. quadricarinatus crayfish were detected in places upstream of the introduction point described in this study. This might be related to lower water temperatures, predators, physical barriers or fishing pressures as reported other places (Nunes et al. 2017). Dispersal of C. quadricarinatus across streams, irrigation canals and floodplains has been reported in other parts of the world. The dispersion rate of 2.2 km/year is shorter than 6.6 km year on average, which is what has been reported for this species in other environments (Nunes et al. 2017). This is due to the network of channels found in the area. The introduction of C. quadricarinatus later in 2001 for culture purposes in the other three sites could accelerate its propagation rate in the study area, ensuring the success of its invasion (Lockwood et al. 2005), and acting as stepping stones into previously un-invaded areas (Johnson et al. 2008). Cherax quadricarinatus is an invasive species, and there are reports of the establishment of its wild populations in several tropical and subtropical countries (Snovsky and Galil 2011). In this study, it is confirmed that populations of C. quadricarinatus are established in the coastal plain of San Blas, Nayarit State, and have spread to different localities as far as 37 km from the point of introduction. This species can be considered as fully invasive (category E), according to Blackburn et al. (2011). Since C. quadricarinatus in the study area grows, survives and reproduces in multiple sites with a greater spectrum of habitats, it is classified as an invasive species with a wide distribution rate (CABI 2019), causing a minor impact (MI) on competition, predation, transmission of diseases to native species, parasitism and grazing/herbivory/browsing according to the criteria of Blackburn et al. (2014). The study area is used for various land purposes such as accelerated urban, tourism, agricultural, aquatic and fishing development, thus putting the freshwater and brackish ecosystems under increasing pressure from the loss of habitat, pollution, overexploitation, species invasion, and climate change. However, the ecological impacts of the introduction of C. quadricarinatus were not well studied, even though global experiences have shown that other crayfish have altered freshwater environments (Lodge et al. 2012; Twardochleb et al. 2013). The most obvious effects have been that they modify the abundance of macrophytes and accelerate the breakdown of detritus in floodplain ecosystems in the invasion zone (Nunes et al. 2017). Alien populations of C. quadricarinatus established in the coastal ecosystems of Nayarit have increased and they are now been exploited for commercial purposes in the region by establishing an artisanal fishery that has improved the income of fishermen in the study area (Ponce-Palafox et al. 2012). This has the potential to put pressure on the native Caridean

Tapia-Varela et al. (2020), BioInvasions Records 9(2): 357–366, https://doi.org/10.3391/bir.2020.9.2.21 363 Establishment of Cherax quadricarinatus in the Coastal Plain of San Blas

populations of the Macrobrachium by limiting their distribution and abundance (Ponce-Palafox et al. 2002, 2009) and can displaced the freshwater (Parathelphusa maculata) in streams where they co-occur, as reported in Southeast Asia (Zeng et al. 2019). The introduction of exotic aquatic species such as C. quadricarinatus in the coastal plain of San Blas, Nayarit State for commercial exploitation and human consumption, should be subject to Mexican environmental regulations (NOM-000-ZOO 2009; NOM-059-SEMARNAT-2010). The great invasive potential of this species can cause changes in the structure, diversity, and organization of trophic functional groups in ecosystems where the native species live. The introduction of this species has created opportunities for social welfare through the commercialization of a new and successful fishery. However, we need to consider that such introduction carries with it an environmental risk of displacing endemic species, and the resulting potential for ecological disasters makes such an introduction a crime against the environment.

Acknowledgements

We sincerely appreciate Reforma Agraria for being cordial and kind during the development of this research: Lucio Jara, Gregorio Jara, Samuel Jiménez, Eleuteria Tapia, Toño Tapia, and Gerónimo Tapia, and all the co-workers during sampling. We are particularly thankful to Esmeralda Varela, Merced Tapia and sons, relatives of the first author. Without their support, confidence and help, it would have been practically impossible to carry out this research. We are grateful to the reviewers who provided useful comments on an earlier draft of the manuscript.

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