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Home , Cichla monoculus, Sea of Galilee, Tiberias

BioInvasions Records (2019) Volume 8, Issue 3: 706–711

CORRECTED PROOF

Rapid Communication The occurrence of the (Cichla kelberi Kullander and Ferreira, 2006) in Kinneret ( of ),

Daniel Golani1,*, Oren Sonin2, Gregory Snovsky3, Lior David1,4 and Roni Tadmor-Levi1,4 1National Natural History Collections and Department of Ecology, Evolution and Behavior, The Hebrew University of , 91904 Jerusalem, Israel 2Department of Fisheries, Ministry of Agriculture. P.O. Box 1213 Kiryat Haim, 26105 Israel 3Fishery Department, Ministry of Agriculture and Rural Development, Dona Gracia 6, 14100, Israel 4Department of Sciences, RH Smith Faculty of Agriculture Food and Enviroment, The Hebrew University of Jerusalem, , Israel Author e-mails: [email protected] (DG), [email protected] (OS), [email protected] (GS), [email protected] (LD), [email protected] (RT-L) *Corresponding author

Citation: Golani D, Sonin O, Snovsky G, David L, Tadmor-Levi R (2019) The Abstract occurrence of the peacock bass (Cichla kelberi Kullander and Ferreira 2006) in A specimen of Cichla kelberi Kullander and Ferreira, 2006 was captured for the first Lake Kinneret (), Israel. time from Lake Kinneret (Sea of Galilee or Lake Tiberias), Israel. Its identification BioInvasions Records 8(3): 706–711, was made by morphological and molecular means. Although importation of this https://doi.org/10.3391/bir.2019.8.3.28 species to Israel is prohibited, commercial importers have smuggled juveniles as Received: 1 March 2019 aquarium fish. The introduction vector of the specimen in Lake Kinneret is Accepted: 3 June 2019 probably due to release or escape from the aquariums of hobbyists. Published: 4 July 2019 Key words: exotic, freshwater fish, Lake Tiberias, Cichlidae Handling editor: Darragh Woodford Thematic editor: Michal Janáč Copyright: © Golani et al. Introduction This is an open access article distributed under terms of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0). The introduction of fish species, whether intentional or unintentional, may OPEN ACCESS. have a negative impact on local communities (Pelicice and Agostinho 2009; Sharp et al. 2017). The risk of damage to the structure of the native ichthyofauna is much greater in freshwater than in the marine environment since freshwater populations are often very small, restricted to a limited geographic and have a high rate of endemism (Maitland 1995). Lake Kinneret (The Sea of Galilee or Lake Tiberias) is a monomictic lake situated in the Syrian-African Rift Valley. Its length is 21 km and its width 2 3 13 km; its surface area is 168.9 km , volume of 4.13 km and maximum depth is ca. 47 m. It is the lowest freshwater lake in the world and experiences great fluctuations of its water level, from a maximum of −209 m to close to −215 m below in recent years. The exotic ichthyofauna of the Israeli freshwater ecosystem have been studied by Goren and Ortal (1999), Golani and Mires (2000) and Roll et al. (2007). Golani and Mires (2000) enumerated 17 exotic species in Lake Kinneret, of which only two (common Cyprinus carpio and mosquito fish Gambusia affinis) have established vital populations in the lake. In subsequent years, additional exotic

Golani et al. (2019), BioInvasions Records 8(3): 706–711, https://doi.org/10.3391/bir.2019.8.3.28 706 Peacock bass from Lake Kinneret, Israel

Figure 1. The specimen of Cichla kelberi (HUJ 20912) caught in Lake Kinneret on 26 November 2018.

species were recorded from Lake Kinneret: Striped Pangasius hypophthalmus (Pangasidae), suckermouth armored catfish Pterygoplichthys pardalis (Loricaridae) and the giant snakehead Chana micropletes (Channidae) (Snovsky and Golani 2012; Golani and Snovsky 2013; Golani et al. 2015, respectively). All these species were recorded as a single specimen.

Materials and methods On 26 November 2018, a 298 mm SL (362 mm TL) specimen of the genus Cichla was caught by commercial trammel net in Lake Kinneret, Israel. The specimen was photographed while fresh (Figure 1); later it was damaged by the fishermen, prior to purchase by the authors, and deposited in the National Fish Collection of the Hebrew University of Jerusalem, where it received the catalogue number HUJ 20912. The specimen was identified according to Kullander and Ferreira (2006) to be Cichla kelberi Kullander and Ferreira, 2006. We preformed the following genetic study: Total genomic DNA was extracted from muscle tissue (Standard phenol-chloroform DNA extraction (Sambrook and Russell 2006)). A 470 bp fragment of the mitochondrial DNA barcode gene cytochrome oxidase I (COI) was sequenced and analyzed. The DNA barcode region was amplified and sequenced following protocols described by Borovski et al. (2018), using primers developed by Ward et al. (2005) (cox1a_fw: 5’-TCAACCACCCACAAAGACATTGG CAC-3’ and cox1a_rv: 5’-TAGACTTCTGGGTGGCCAAAGAATCA-3’).

Golani et al. (2019), BioInvasions Records 8(3): 706–711, https://doi.org/10.3391/bir.2019.8.3.28 707 Peacock bass from Lake Kinneret, Israel

Figure 2. The DNA sequence of 470 bp fragment of the mitochondrial DNA barcode gene cytochrome oxidase I (COI) for specimen of Cichla kelberi (HUJ 20912).

After removal of low quality sequence at the 5’ and 3’ ends a 470 bp DNA barcode was obtained (Figure 2) and deposited in the GenBank with the accession number MK550509. The sequence was also queried using basic local alignment search tool (BLAST; http://blast.ncbi.nlm.nih.gov/Blast.cgi/), against NCBI nucleotide database.

Results The finding of Cichla kelberi constitutes the first record of this species from the Israel freshwater ecosystem.

Brief description of the Kinneret specimen (HUJ 20912) Body moderately deep and slightly compressed. Large head (39.3% of SL) with a large, slightly slanted mouth. The lower jaw is projected. Both jaws with a band of minute teeth, which extend back vertically close to the anterior of eye. A single dorsal fin with 15 spines and 17 rays with a distinct notch between the spinous and the ray parts. Last dorsal spine almost twice in length than the penultimate spine. Anal fin with three spines and 11 rays, its origin under the 7th dorsal ray. Pectoral fin with 14 rays and pelvic fin with one spine and five rays. Caudal fin slightly rounded. Discontinuous lateral line; the upper part ends below the first dorsal ray, while the posterior part begins below the penultimate dorsal spine and ends at the base of caudal fin. Color: Body is olive-green with yellowish-red belly, lower jaw and lower part of caudal fin. Black and yellow dots on the lower vent. A distinct dark spot surrounded by a yellow ring at the base of caudal fin. The eye is surrounded by an orange ring. Three horizontal dark bars; the first under the spinous part of dorsal fin, the second under the notch between the spinous and the ray part of dorsal fin and the third under the middle of the ray portion of dorsal fin. Faded occipital bar. Anal and caudal fins immaculate.

Golani et al. (2019), BioInvasions Records 8(3): 706–711, https://doi.org/10.3391/bir.2019.8.3.28 708 Peacock bass from Lake Kinneret, Israel

Table 1. Polymorphic bases compared to the 470 bp sequence of the Kinneret specimen (HUJ 20912) and Cichla kelberi and C. piquiti. Species/position Acc. 12 86 152 163 171 200 258 269 428 437 447 Reference HUJ 20912 MK550509 C C T T A A T T C C A Cichla kelberi JN988796/7 G C T C G G T T T C G (Pereira et Cichla piquiti JN988800 G T C C G A C C C T A al. 2013)

The genetic analysis showed closest matching results belonged to COI sequences of Cichla kelberi (Accessions JN988796/7) and Cichla piquiti (Accession JN988800) with 98.73% and 98.3% identity, respectively (Table 1).

Discussion The family of Cichlidae includes 1762 species in 202 genera (Nelson et al. 2016). The genus Cichla occurs naturally only in the freshwaters of and consists of only 15 species. The of the genus Cichla is very complicated, resulting in a plethora of misidentifications and synonymizations. In their comprehensive revision of the genus, Kullander and Ferreira (2006), using morphological characteristics, described nine new species, in addition to the six nominal species that were known prior to their publication. Following this study a molecular assessment by Willis (2017) postulated that there are several more cryptic species. Moreover, Brinn et al. (2004) showed that hybridization of congeneric species occurs naturally. Cichla kelberi is morphologically similar to C. monoculus and C. pleiozona. It can be distinguished from the former by the absence of light spots on the anal and pelvic fins and from the later by the presence of a lateral band from the head to the caudal fin and a dark vertical bar on the anterior part of the caudal peduncle (Kullander and Ferreira 2006). Genetic results excluded the possibility that the Kinneret specimen belonged to either of these two species (C. monoculus and C. pleiozona), as they do not occur in areas from which the closest matching sequences originated (see Fig. 4 in Pereira et al. 2013 as compared to Figs. 9 and 23 in Kullander and Ferreira 2006). The genetic results showed that the Kinneret specimen was found to be Cichla kelberi which is closest to C. piquiti. However, C. piquiti can be distinguished from C. kelberi by having several rows of light spots on the ray portion of dorsal fin and the upper lobe of caudal fin. Cichla kelberi is native from Brazilian but was introduced to many watersheds (Espinola et al. 2010; Ortega et al. 2015). Like other members of the genus, its juveniles and young feed on small invertebrates, mainly shrimps, while adults are piscivorous (Breder and Rosen 1966). Eggs are deposited on hard substrate. After hatching, both parents transfer the larvae by mouth to a small nest prepared in advance (Breder and Rosen 1966). The source of the Lake Kinneret specimen is evidently an aquarium release or escapee. All species of the genus Cichla are popular in the aquarium trade (Kullander and Ferreira 2006) and prohibited for import to Israel, thus making recreational anglers an unlikely vector. However, importers often try

Golani et al. (2019), BioInvasions Records 8(3): 706–711, https://doi.org/10.3391/bir.2019.8.3.28 709 Peacock bass from Lake Kinneret, Israel

Figure 3. Three specimens of Cichla kelberi (HUJ 20908), 66–72 mm SL, that were confiscated on 28 June 2018 at Ben-Gurion International Airport. Photo by D. Golani.

to smuggle in juveniles and young specimens, which are highly valued despite their large adult size making them high risk species for illegal aquarium dumping (Magalhães et al. 2017). The local authorities often catch and confiscate these illegal specimens. Figure 3 shows three young specimens (66–72 mm SL) that were confiscated on 28 June 2018, among more than two dozen at Ben-Gurion International Airport. They were preserved at the Fish Collection, National Collection of the Hebrew University and received the catalogue number HUJ 20908. The main concern for the management of Lake Kinneret is whether the collection of HUJ 20912 is an isolated incident or whether more specimens were introduced into the lake and if they are capable of reproducing in the local environment and establishing vital populations. If C. kelberi does establish an exotic population in the Lake, this top predator could cause declines in fish community diversity, as documented elsewhere (Pelicice and Agostinho 2009; Sharp et al. 2017), and thus possibly constituting a significant threat to the Kinneret system. The winter temperature in the Lake drops to 14–17 °C during winter in the pelagic zone, which is below

Golani et al. (2019), BioInvasions Records 8(3): 706–711, https://doi.org/10.3391/bir.2019.8.3.28 710 Peacock bass from Lake Kinneret, Israel

the known tolerance of this species (25–28 °C; Froese and Pauly 2019). However, there are several warm springs fluxing through the bottom of the lake that could serve as refuge sites during the winter.

Acknowledgements

We would like to thank the anonymous reviewers for their comments and suggestions.

References

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