Open Access
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 419, 2018
Article Number 14
Number of page(s) 5
DOI https://doi.org/10.1051/kmae/2018004
Published online 06 March 2018

© A. Jabłońska et al., Published by EDP Sciences 2018

Licence Creative Commons
This is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (http://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

Human-mediated introductions of alien species into fresh waters is a well-known phenomenon world-wide. Tropical and subtropical organisms are able to inhabit thermally polluted water bodies of the temperate zone (Maczulak, 2010). In Europe, classic examples of alien invertebrates thriving in water bodies with elevated water temperatures include Branchiura sowerbyi (Oligochaeta) and Sinanodonta woodiana (Bivalvia), both originating from tropical and subtropical Asia (Gruszka, 1999, Kraszewski and Zdanowski, 2011, Jabłońska et al., 2015).

The shrimp Neocaridina davidi (Bouvier, 1904) occurs naturally in fresh waters of South-East Asia (Cai 1996). It has already been introduced to Hawaii (Englund and Cai, 1999) and Japan (Nishino and Niwa, 2004). In Europe, this species is an extremely popular aquarium pet (Nur and Christianus, 2013, Horwath, 2015, Pantaleão et al., 2017) but was only recently found in nature, in thermally polluted tributaries of the River Rhine, Western Europe (Klotz et al., 2013).

In this study, we provide a first report on the occurrence of N. davidi in Poland, Central Europe. The shrimp were collected in a ca. 4.5 km-long artificial canal connected to the lower section of the Oder River, south of Gryfino (N 53°12′42.36″, E 14°28′2.70″). The canal receives heated waters from the large Dolna Odra Power Station cooling system. Bottom sediments at the sampling site were composed of fine-grained sands and mud. The banks were partially covered by concrete. The water temperature at the sampling site in June − July was 27–29 °C, while in November, it dropped to 15 °C. A total of 15 animals were found in qualitative benthic samples, collected using a hydrobiological hand-net from submerged vegetation in July 2003 (3 individuals), November 2013 (3 ind.) and June 2017 (9 ind.). The sample from June 2017, was taken from a 1 m2 surface in about 15 min sampling time. For comparison and taxonomic verification, in 2017, we acquired six specimens of N. davidi var. “Red Cherry” from an amateur aquarium culture in Łódź, Poland, ca. 500 km south-east from the sampling site. All individuals, except the sample from 2003 (which was preserved in 4% formaldehyde), were instantly preserved in 96% ethanol.

Morphological examination of shrimp was carried out using descriptions in papers by Englund and Cai (1999) and Klotz et al. (2013). Individuals were then DNA-barcoded using the cytochrome c oxidase subunit I (COI) marker. Total DNA was extracted from the abdominal tissue of 13 specimens, collected both from the field and from aquarium using the Chelex procedure (Casquet et al., 2012). The PCR reaction followed the protocol provided by Hou et al. (2007), with the primer pair HCOJJ/LCOJJ (Astrin and Stüben, 2008). PCR products were purified with Exonuclease I and FastAP alkaline phosphatase (Werle et al., 1994), and then sequenced by Macrogen Inc., Korea. The obtained sequences are deposited in GenBank (Benson et al., 2005). The GenBank accession numbers are provided in Table 1. In addition, we acquired five COI sequences of Neocaridina davidi from Taiwan and Hawaii, published and deposited in GenBank, under the name Neocaridina denticulata sinensis (Kemp, 1918), by Shih and Cai (2007) (Tab. 1). The sequences were aligned and trimmed to the length of 610 bp in Geneious 6.1.8 (Kearse et al., 2012). Haplotypes were identified using the DnaSP software (Librado and Rozas, 2009). The Neighbour-Joining method was applied using Mega 7.0 (Kumar et al., 2016). Caridina cantonensis COI sequence was chosen as an outgroup (Tab. 1).

The material examined morphologically, contained five males and 16 females (one ovigerous, collected in November 2013). All individuals were identified morphologically as Neocaridina davidi using the following characteristics (based on all the individuals found at the sampling site). Body length, 13 to 24.5 mm. Average body length of males: 15.5 mm, average body length of females: 19.3 mm. Rostrum, with 13–18 dorsal teeth (2–4 postorbital) and 4–8 ventral teeth, reaching the distal edge of the third antennular segment. The tip of the rostrum slender, slightly curved, without teeth. Eyes, normally developed. Carapace smooth. Supraorbital spine absent. Antennal spine well-developed. Pterygostomian angle acute and sharply pointed. Pereiopods normally developed, characteristic of the family Atyidae. Spines on dactylus of the 3rd pair of pereiopods in males stronger and thicker than in females. Endopod of the 1st male pleopod, pear-shaped, broad and rounded in its distal part. Telson, shorter than uropods, with 4–5 pairs of dorsal spines, margin rounded, armed with 8–10 long spines.

DNA COI barcodes also confirmed that all the studied shrimps belong to Neocaridina davidi. The haplotype assignment showed that all the individuals, collected either in the wild or from the aquarium culture, belonged to a single haplotype (Fig. 1). Moreover, four other COI haplotypes of individuals from Hawaii and Taiwan, acquired from GenBank, differed from the sequences we obtained, by only one to three mutations.

The results of our morphological and genetic analyses confirms the presence of N. davidi in the thermally-polluted canal connected to River Oder near Gryfino, Poland. Low numbers of shrimp found in the samples may indicate low abundance and density. The population in the sampling site is distributed pointwise and it is probable that numerous suitable habitats are inaccessible for sampling, enclosed in the Power Plant’s grounds. This is the second record of this species, from European surface waters and the first from Central Europe. Neocaridina davidi is the second freshwater shrimp species reported from Poland after Atyaephyra desmarestii recorded previously from the western, natural, branch of the Oder River near Gryfino (Gruszka, 2001). Although both shrimps, N. davidi and A. desmarestii, belong to family Atyidae, the differences in their morphology are clear (Klotz et al., 2013).

Neocaridina davidi, particularly the variety “Red Cherry”, is a very popular aquarium pet world-wide, including Europe (Nur and Christianus, 2013, Horwath, 2015, Pantaleão et al., 2017). We propose that, as in the Rhine tributaries in western Germany, the population occurring in the canal near Gryfino derives from an aquarium culture, especially since the wild individuals share the same haplotype as the cultured ones. Moreover we cannot exclude the possibility that the population has been settled in this place for more than a decade. The individuals (including one ovigerous female) were collected in 2003, 2013 and 2017, the temperature in the canal reaches 27–28 °C, which are the most favorable values for breeding of N. davidi (Nur and Christianus, 2013, Tropea et al., 2015). Another possibility, although less probable over such a long period, would be a series of yearly introductions supplying the population regularly with captive-bred individuals. Thus, the population should be investigated in the coming years to check its stability at the study site. It would be also interesting to study a wider area to ascertain if the species is spreading.

Although releasing aquarium pets into open waters can be harmful for natural ecosystems, this phenomenon is quite common (Gherardi et al., 2007, Lipták and Vitázková, 2015). Aquarists often believe this is a more humanitarian solution than killing unwanted pets (Duggan, 2011). In some cases, stable populations of exotic species pose a threat to native species and entire ecosystems including increased predatory pressure on indigenous fauna or introduction of new diseases or pathogens (Gherardi et al., 2007, Klotz et al., 2013, Weber and Traunspurger, 2016). So far, no such threats associated with N. davidi have been found in nature. On the other hand, most tropical organisms introduced to natural waters in temperate climates are not able to survive the winter. Some, however, do find the new conditions advantageous. Klotz et al. (2013) noted that the native habitat of N. davidi is not tropical, since the water temperatures range from 6 °C in winter to 30 °C in summer. Such winter temperatures are still 2–4 °C higher than those in Central Europe (Wetzel, 2001). Nevertheless, the global warming associated with prolonged periods without cold spells in winters and heat waves in summers (Anders et al., 2014), makes the temperate zones more prone for acclimatization of thermophilic species. Such is the case of the predominantly Mediterranean scarlet dragonfly, Crocothemis erythraea (Brullé, 1832), recently expanding its breeding range in Central Europe (Ott, 2010). We suppose that thermally polluted water bodies may serve as gateway ecosystems in which such species adapt to local conditions and, in the future, colonize natural waters. After acclimatization, the further spread of alien freshwater species is usually promoted by other human activities, such as building artificial channels connecting previously isolated river basins, inland waterway transportation, tourist movement as well as by ecosystems degradation (Gherardi, 2007). Thus, we suspect that, with increasing propagule pressure from amateur aquarists, further climate warming and connection of inland waterways, N. davidi will likely spread in Central Europe and become a stable element of local fauna, as the thermophilic Procambarus clarki (Girard, 1852) has in many other regions of Europe (Souty-Grosset et al., 2016). It would be beneficial to promote the education and awareness of the problems of releasing non-native aquarium species into water systems. This activity is an adverse procedure for natural environments, particularly because controlling such activities is very difficult.

Acknowledgements

The study was supported by the internal funds of the University of Lodz. We would like to thank Andrzej Zawal (University of Szczecin) and Jacek Sadowski (West Pomeranian University of Technology Szczecin) for providing some material used in this study. Finally, we would like to thank dr. Tammy Horton, National Oceanography Center, Southampton, UK, for the language corrections.

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Cite this article as: Jabłońska A, Mamos T, Gruszka P, Szlauer-Łukaszewska A, Grabowski M. 2018. First record and DNA barcodes of the aquarium shrimp, Neocaridina davidi, in Central Europe from thermally polluted River Oder canal, Poland. Knowl. Manag. Aquat. Ecosyst., 419, 14.

All Tables

Table 1

Sequences used in analysis

All Figures

thumbnail Fig. 1

Neighbour-Joining tree constructed for newly obtained and GenBank-stored sequences of Neocaridina davidi.

In the text

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