Aquatic Invasions (2008) Volume 3, Issue 2: 181-185 doi: 10.3391/ai.2008.3.2.8 Open Access

© 2008 The Author(s). Journal compilation © 2008 REABIC

Research Article

First record of red swamp , clarkii (Girard, 1852) (Crustacea: : ) in Israel – too late to eradicate?

Gil Wizen1, Bella S. Galil2*, Alex Shlagman1 and Avital Gasith1 1Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel 2National Institute of Oceanography, Israel Oceanographic & Limnological Research, POB 8030, Haifa 31080, Israel *Corresponding author E-mail: [email protected]

Received: 12 May 2008 / Accepted: 23 May 2008 / Published online: 22 June 2008

Abstract

The recent findings of the red swamp crayfish, , in groundwater-filled pits in an abandoned quarry (Hadera, central coastal plain) constitute the first record in the wild of this notoriously invasive in Israel. Crayfish had been offered for sale in local pet shops: twenty years ago several illegally imported specimens had been confiscated by the Israel Nature and Parks Authority and two of the specimens were deposited at the National Collections, Tel Aviv University. The recent finding of a small reproducing population established in a semi natural habitat in Israel raises great concern regarding the potential widening of its range and of the limited options for its eradication. Key words: Procambarus clarkii, Cambaridae, invasive alien species, Israel, eradication

Introduction the largest invertebrate predator in their habitats. They are considered both key-species and Israel’s lotic and lentic habitats have been ecosystem engineers (Statzner et al. 2003; Creed profoundly altered in the past century by and Reed 2004). Crayfish do not occur in Israel's irrigation, drainage and pollution (Gasith 1992), inland water. The recent findings of the red and the intentional and unintentional intro- swamp crayfish, Procambarus clarkii (Girard, duction of alien species has harmed the already 1852), in ponds on the central coastal plain, embattled native biota (Roll et al. 2007a, b). raises great concern, because this is Forty-one fish species have been introduced into widely regarded as an that Israel’s freshwater habitats unintentionally and adversely impact aquatic ecosystems (Barbaresi for aquaculture, ornamental purposes, pest and Gherardi 2000; Gherardi 2006). control, improvement of wild stock (Goren and Ortal 1999; Golani and Mires 2000; Goren and Galil 2005; Roll et al. 2007b). Only a single Material and methods alien decapod crustacean, the American blue Study site , Rathbun, 1896, has been reported from Israeli inland water. The blue Several ponds at the site of an abandoned quarry crab, though unable to reproduce in freshwater, (located 2 km south-west of the Hadera-West has been repeatedly introduced into the Sea of train station, 32.42328°N and 34.88725°E) were Galilee with fish fry caught along the Medi- examined as part of a survey of the amphibian terranean coast and used for restocking the lake fauna of Israel undertaken by the Inland Aquatic (Snovsky and Galil 1990). Laboratory at Tel Aviv University. The largest Freshwater crayfish are often an important water body is a perennial, groundwater-filled pit, component of the aquatic fauna, frequently being measuring ca. 180 x 100 m (Figure 1). At the end

181 G. Wizen et al.

australis Scham., spiny rush, Juncus acutus L., and Tamarix sp). A smaller pond, (ca. 70 m in diameter) is connected to the larger one via a short channel. Schools of cichlids (Tilapia sp.) and mosquitofish, Gambusia affinis (Baird and Girard, 1853), were sighted in the latter. Fishing nets sighted along the pond's margin raise the suspicion that the ponds were used for illegal Figure 1. Groundwater-filled pit, banks with riparian aquaculture. Ephemeral rain-pools (ca. 10-20 m vegetation, Hadera-West site. Photograph by Gil Wizen. in diameter, 30 cm deep, salinity 1 psu) are located less then 100 m east and north of the groundwater-filled pit (Figure 2). These rain- pools are the home for seasonally flourishing aquatic invertebrates (e.g., flatworms, entomo- stracan , aquatic insects, gastropods) and 3 species of amphibians (Hyla savignyi Audouin, 1827, Bufo viridis Laurenti, 1768 and Rana ridibunda Pallas, 1771).

Survey for Procambarus clarkii The first recording of the crayfish (March 11th, 2008) was fortuitous. Since then the perennial and ephemeral water bodies were visited 8 times over a 3 month period (including 2 night visits; daytime: March 11th and 21st, April 7th, 14th, Figure 2. Rain-pool, Hadera-West site, 4 March 2008. Photograph by Gil Wizen. 21st and 28th; nighttime: March 26th and May 6th). The crayfish were sampled by hand to avoid damage that often occurs when dip-netted. Five specimens were preserved (70% ethanol), Table 1. The list of P. clarkii specimens preserved at the identified and deposited in the Tel-Aviv National Zoological Collections, Tel Aviv University. University Zoological Museum (ZMTAU). Carapace Collection Sex length Catalogue number date Results (mm) ♀ 44.2 1988 AR 28358 Procambarus clarkii adults' and juveniles' molts ♂ 52.1 1988* AR 28359 were first collected on March 11th, 2008. In ♂ 38.3 21.03.2008 AR 28360 subsequent samplings ca. 30 specimens adults ♂ 30.6 21.03.2008 AR 28360 and juveniles were collected and released except ♂ 33.9 21.03.2008 AR 28360 for 5 live specimens and a molt that were ♂ 33.1 21.03.2008 AR 28360 transferred to the laboratory for identification. ♀ 31.9 21.03.2008 AR 28360 During the night surveys tens of adults and Molt 56.7 11.03.2008 AR 28361 juveniles were observed on the bottom of the *The specimen had been kept for two years in a freshwater smaller perennial pond. The collected specimens aquarium. were identified as Procambarus clarkii, sexed and measured from the apex of the rostrum to the mid-dorsal posterior margin of carapace (Table of the rainy season the water level exceeds depth 1). Larger specimens were observed (Figure 3A) of 1 m. The water level and the pond's size but not measured. A female and 4 males were gradually diminish in summer. The water is deposited at the National Collections (ZMTAU). brackish (salinity 2.8 psu), and clear. The bottom On one occasion (April 7th, 2008) a live is sandy and the banks are covered by riparian specimen was observed on land underneath vegetation (the common reed, Phragmites a plastic bag, at a distance of ca. 10 m from a australis (Cav.) Trin. ex Steud., cattail, Typha rain-pool. The rain-pools dried early this year

182 First record of red swamp crayfish in Israel

due to a severe drought. On April 21st the rain- pools were already dry and several individuals of P. clarkii were observed digging burrows under stones (Figure 3B). On April 28th, two males (Figure 3C) and two females (one gravid, Figure 3D), were removed from a single burrow, at least 20 cm deep. On May 2nd, the dried up rain-pool was searched again for burrowing crayfish. Three specimens were found alive, each in a separate waterlogged burrow that was topped by wet soil. Three other specimens were found dead in their burrows. We attribute the latter to the failure of the crayfish to reach groundwater due to rocky strata that blocked their way.

Discussion

Procambarus clarkii, native to northeastern and south-central U.S.A (Hobbs 1989) has been widely introduced since the mid 20th century because of its commercial value in aquaculture (Hobbs et al. 1989). Following intentional release or unintentional escape from farms the crayfish entered and colonized natural water bodies forming self-sustaining populations in the wild (Gherardi 2006). The life history traits that endear the species to the aquaculture industry – rapid growth, high fecundity, poly- trophism, resistance to disease and to pollution and extreme environmental conditions – make it an invincible invasive (Barbaresi and Gherardi 2000). It is known to tolerate drought periods, low oxygen concentrations (2 mg/l), a relatively wide range of salinity and temperature (5-38ºC) (Gutiérrez-Yurrita et al. 1999). Spain was the first peri-Mediterranean country to introduce the species in 1973 (Habsburgo-Lorena 1979). In 1979 P. clarkii was reported from Portugal (Ramos and Pereira 1981); in the early 1980s in Egypt (El Zein 2005) and since 1990 in Italy (Gherardi et al. 1999). Recent studies supported previous observations that P. clarkii is capable of flourishing in most types of water bodies, including small, ephemeral ones, and anthropo- genically-disturbed habitats. There is evidence that the crayfish is able to move overland and thereby increase its range (Aquiloni et al. 2005; Cruz and Rebelo 2007). Israel's natural water bodies are already stressed by the diversion of water for human use Figure 3. Procambarus clarkii: A – a large male, observed on 6 May 2008, night survey; B - in a water-filled burrow, (Gasith 1992). Penetration of an invasive, large, 28 April 2008; C - two males observed at the mouth of a opportunistic, omnivorous predator such as burrow, 28 April 2008; D - a gravid female, 28 April 2008. P. clarkii further stresses the aquatic ecosystems. Photographs by Gil Wizen Furthermore, in Israel P. clarkii has no known

183 G. Wizen et al. predator and is likely to become a predominant There is no doubt that P. clarkii poses a species in these ecosystems. The exertion of high serious threat to the native aquatic biota in predation pressure may result in irreparable Israel. If indeed the Hadera population is an damage to the native aquatic biota (Pérez-Bote isolated self-maintaining one, all efforts should 2005; Rodríguez et al. 2005; Geiger et al. 2005; be made to eradicate it. We suggest that prompt Gherardi and Acquistapace 2007). Especially action be taken to eradicate or at least control vulnerable are the eggs and tadpoles of this population, either by applying physical amphibians breeding in ephemeral ponds. It has means for removal or the use of organophosphate been proposed that invasion of P. clarkii may insecticides (after consulting the National Water have played an important role in structuring Authority experts). Applying the insecticide amphibian communities in temporary ponds. while the crayfish population is small and at the Presence of this species in the water body may time the water bodies are at their lowest water force the amphibians to marginal and isolated level, may reduce the amount of biocide needed. habitats, reducing their reproductive success, ultimately leading to local extinctions (Cruz and Acknowledgements Rebelo 2005; Cruz et al. 2006a, b). A case in point is the impact of the introduction of We acknowledge the assistance of Dr. Ilan Karplus in the P. clarkii to Egypt. A farmer in Al identification of the crayfish. The permit to survey the water Qanater released the imported crayfish into the bodies was issued by the Nature and Parks Authority of Israel. Nile in the 1980s after they had damaged the mud banks of his ponds. The crayfish have since spread from the Delta to Bani Swaif, 500 km to References the south of Cairo, with densities as high as 0.65/m2 (El Zein 2005). The crayfish damaged Aquiloni L, Ilhéu M, Gherardi F (2005) Habitat use and earth dams, irrigation canals and fish stock, and dispersal of the invasive crayfish Procambarus clarkii in ephemeral water bodies of Portugal. Marine and though marketed, are considered of little Freshwater Behaviour and Physiology 38(4): 225-236, commercial value. El Zein (2005) admits “such http://dx.doi.org/10.1080/10236240500310195 an introduction is now recognized to have bad Barbaresi S, Gherardi F (2000) The invasion of the alien crayfish Procambarus clarkii in Europe, with particular consequences on biodiversity without economi- reference to Italy. Biological Invasions 2: 259-264, cal profits”. http://dx.doi.org/10.1023/A:1010009701606 Once widespread, aquatic aliens are difficult if Chang VCS, Lange WH (1967) Laboratory and field not impossible to be rid off. Unless detected evaluation of selected pesticides for control of the red crayfish in California rice fields. Journal of Economic early enough, their eradication may become Entomology 60: 473-477 impractical. If proven isolated in one site, the Creed RP, Reed JM (2004) Ecosystem engineering by decimation of P. clarkii population in Israel may crayfish in a headwater stream community. Journal of the North American Benthological Society 23: 224-236, still be possible, reducing the risk of spreading to http://dx.doi.org/10.1899/0887-3593(2004)023<0224:EEBCvIA other water bodies. However, decimation and >2.0.CO;2 certainly eradication are by no means an easy Cruz M J, Pascoal, S, Tejedo M, Reblo R (2006a) Predation task. Organophosphate insecticides have been by an exotic crayfish Procambarus clarkii, on natterjack toad, Bufo calamita, embryos: its role on the exclusion of proven effective in laboratory and large-scale this amphibian from its breeding ponds. 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