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Communication

New Records of the Alien Chinese Ricefish (Oryzias sinensis) and Its Dispersal History across Eurasia

by
Alexander A. Makhrov
1,*,
Valentina S. Artamonova
1,
Yue-Hua Sun
2,
Yun Fang
2,
Andrey N. Pashkov
3 and
Andrey N. Reshetnikov
1
1
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskiy pr. 33, 119071 Moscow, Russia
2
Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
3
Krasnodar Department of the Azov-Black Sea Branch of the VNIRO (AzNIIRKh), 350000 Krasnodar, Russia
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(3), 317; https://doi.org/10.3390/d15030317
Submission received: 19 December 2022 / Revised: 13 February 2023 / Accepted: 18 February 2023 / Published: 21 February 2023
(This article belongs to the Special Issue Aquatic Organisms Diversity and Bio-Indication of Water Resources—2nd Edition)
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Abstract

:
The diversity of biota in different parts of the planet has demonstrated dramatic changes within the last several decades due to the extinction of native taxa and the appearance of invasive taxa. The correct taxonomic identification of non-native species is important for understanding their dispersal abilities, especially when potential invaders may be of closely related species. Information on the species identity of ricefish (Oryzias spp.), which have formed self-sustainable populations in some parts of Eurasia, is contradictory. In this paper, we studied samples from non-native populations of Oryzias from several Eurasian regions. The results of our mtDNA COI partial sequence study confirm that the individuals we studied belong to the species Chinese ricefish, O. sinensis. Analyses of the literature and our own data suggest that all known alien populations of Oryzias in continental Eurasia belong to the same species, O. sinensis. A recent finding of O. sinensis in the Don delta suggests that one of the species’ secondary dispersal pathways could run from the Kuban region through the lower part of the Don basin to the Cis-Azov area.

1. Introduction

The diversity of biota in different parts of the planet has demonstrated dramatic changes within the last several decades due to the extinction of native taxa and the appearance of invasive taxa [1,2,3]. The expansion of invasive organisms outside of their native ranges is a major challenge, as they may affect both the structure and the functioning of native ecosystems, as well as the efficiency of human economic activities [4,5,6]. However, the correct taxonomic identification of alien species is an important prerequisite for assessing the potential damage they may cause, and for tracking the directions and dynamics of their subsequent spread [7,8,9].
At the same time, determining the taxonomic identity of alien species can be difficult if two (or more) closely related, morphologically similar species are potentially involved in the colonization of new territories. In this case, taxonomic identification may be successfully performed by using a molecular genetic approach, which has been applied many times in recent years in order to identify alien freshwater species in different Eurasian regions (e.g., river crayfishes [10,11,12], mollusks [13,14,15], frogs [16], and pathogens to hydrobionts [17,18]).
Presently, in different parts of Eurasia, members of the genus Oryzias, the ricefish, have formed non-native populations. These small fishes, which do not exceed 60 mm in length, belong to the family Adrianichthyidae, of order Beloniformes. The native range of the genus Oryzias extends across areas of continental Asia, from the Korean peninsula to India, and on a number of islands: Japan, Hainan, Taiwan, and the Indo-Malay-Philippines Archipelago [19]. However, these fishes have declined in most of their native range in Asia due to habitat destruction, pesticide use, etc. Oryzias fishes commonly inhabit shallow areas of freshwater bodies overgrown with abundant macrophytes. Their high resilience, small size, and rapid turnover of generations have allowed them to become a model subject for genetic, physiological, embryological, toxicological, carcinogenesis, and behavioral studies [20].
The same characteristics have also allowed Oryzias fishes to become active invaders, and they have significantly expanded their range in recent decades. Representatives of the genus Oryzias have formed numerous self-sustainable populations in water bodies in Kazakhstan [21,22,23], Uzbekistan [24], Turkmenistan [25], the Krasnodar Territory of Russia [26], southeastern Ukraine [27], Japan [28], and two regions of China: the Tibetan Autonomous Region [29] and the Xinjiang Uyghur Autonomous Region [30]. However, the actual species identification of Oryzias from some of the above-mentioned populations has been determined without any deep examination of external morphological and genetic diagnostic features.
To date, 24 species of the genus Oryzias are known, but the taxonomy of the genus is still not well established and remains poorly understood, even in its natural range [19]. Until recently, only one species of Oryzias, i.e., the Japanese ricefish (O. latipes), was assumed to inhabit Japan, the Korean peninsula, and the eastern and southern regions of China [31]. However, in recent years, it has become clear that the O. latipes is restricted to the Japanese islands and the southern part of the Korean peninsula [32], whereas a different species, the Chinese ricefish, O. sinensis, inhabits the western part of the Korean peninsula, as well as eastern and southern China [21,32,33]. More recently, the population of Oryzias from the north-eastern part of Honshu Island was described as a separate endemic species, Oryzias sakaizumii [34]. The fish O. sinensis was originally described, on the basis of morphological features, as the subspecies O. latipes sinensis [35]. Indeed, the morphological differences between the two forms are relatively small and considerably overlap [35,36].
However, the species independence of O. sinensis has now been well proven using genetic methods. For example, the survival of second-generation O. latipes x O. sinensis hybrids has been shown to be reduced [37] and, in addition, different alleles of some protein-coding genes have been detected in these forms [38,39]. More recently, it has been shown that each form is also characterized by its own well-defined cluster of mtDNA haplotypes, both for the complete mitochondrial genome and for the COI gene, which is commonly used to separate closely related species [40,41]. The genetic distance between O. latipes and O. sinensis for the mitochondrial COI gene has been estimated at 14.0% [41], whereas a 2.0% difference is generally accepted as an interspecific difference [42]. This implies that both species can be diagnosed unambiguously, without any overlap, by this characteristic.
A number of papers indicate that populations of Oryzias outside their native range are represented exclusively by the species O. latipes [21,25,28,29], but, at least in some cases [21], this may be due to the use of an outdated view on the taxonomy of this genus which does not consider O. sinensis a separate species. So far, only in Japan have genetic analyses been used to prove that non-native populations of Oryzias belong to the species O. latipes [43]. Other papers credit non-native populations to the species O. sinensis [24,25,27,30,44], but only in one case have the authors confirmed their species identification by morphological analysis [27]; genetic analysis was not performed in any of the cited works to confirm the identity of O. sinensis amongst the studied individuals.
Recent dispersal pathways of representatives of the genus Oryzias across Eurasia are not fully understood. In particular, it is unknown how they have come to occur in the south of Ukraine. Although populations of Oryzias have been described many years ago in the Krasnodar Territory, no Oryzias individuals have been found in the Rostov Region of the Russian Federation, between southern Ukraine and the Krasnodar Territory [45,46]. The occurrence of Oryzias, defined by the authors as O. latipes, in Tibet also seems rather unexpected [29].
Importantly, various species of the genus Oryzias have different behavior [47], and exact species identification is important for their use as model subjects in laboratory experiments, as well as for the correct assessment of their invasive potential in new geographic regions. The aim of this work was to clarify the species identity of representatives of the genus Oryzias from populations that have recently emerged in different regions of continental Eurasia on the basis of their genetic features, as well as to analyze their possible means of dispersal within Eurasia.

2. Materials and Methods

The study was conducted in the water bodies of three distant regions of Eurasia: a pond in the Kagalnik village, in the Azov district of the Rostov Region, Russia; an irrigation canal in the vicinity of the Anastasievskaya village, in the Slavyansk district of the Krasnodar Territory, Russia; and a channel inflowing to the Yarlung Tsangpo (Brahmaputra) river in the Tibetan Autonomous Region, China (Figure 1). Fish were caught using deep nets with 1 mm or 5 mm mesh, anaesthetized, and preserved in 96% ethanol. Detailed information on the localities of the fish samples is presented in Table 1.
To determine the species identity using genetic methods, an analysis of a partial nucleotide sequence of the mitochondrial COI gene was performed, following the procedure described in Artamonova et al. [48]. Total cellular DNA was isolated with the DNA-EXTRAN-2 reagent kit (Synthol, Russia) in accordance with the producer’s instructions.
We obtained a PCR product containing a partial sequence of the mitochondrial COI gene using the Tertsik thermal cycler (DNA Technology, Russia). FishF2 and FishR2 primers were used for the amplification of the corresponding mtDNA region and the sequencing of the resulting PCR product [49]. Amplification was carried out in 25 µL of buffer containing 75 mM Tris-HCl (pH 8.8), 20 mM (NH4)2SO4, 0.1% Tween 20, and 2 mM MgCl2 (Fermentas, Lithuania). The amplification mixture contained approximately 300 ng of total cell DNA, 10 pmol of forward and reverse primers, 200 nmol each of four deoxyribonucleotides, and 0.5–0.7 units of polymerase (Bionem, Russia).
Each sample was sequenced twice, from the forward and the reverse primer. The sequencing reaction was carried out by taking 20 ng of the PCR product and 3.2 pmol of the corresponding primer using ABI PRISM® BigDyeTM Terminator v. 3.1 (Applied Biosystems™, Waltham, MA, USA) reagents, with subsequent analysis of the reaction products on the ABI PRISM 3730 Applied Biosystems sequencer of the Collective Use Center “Genome” from the Institute of Molecular Biology, the Russian Academy of Sciences.
We analyzed the sequencing results using a specialized BioEdit v. 7.0.5. editor (bioedit.software.informer.com›7.0/ accessed on 12 April 2022) and constructed the haplotype networks using Network 5.0.0.1 software (http://www.fluxus-engineering.com accessed on 12 April 2022). Sequences of O. latipes and O. sinensis available from the GenBank International Database were used for comparison (Table 2). Previously, the mitochondrial COI gene was successfully used by Yoon et al. for the precise identification of these two species [40].
Moreover, morphological analysis was carried out on the sampled fish. For this purpose, the number of pectoral fin rays was used, which is accepted as the most contrast morphological feature differentiating O. sinensis and O. latipes. According to the first description of O. sinensis [35], individuals of this species typically have 9 rays in the pectoral fin, compared to 10 rays in O. latipes, and 8 rays in O. minutillus, a species also found in southern China.
Table
Table 2. Summary of the COI gene sequences for the Oryzias latipes and O. sinensis fishes available in the NCBI GenBank.
Table 2. Summary of the COI gene sequences for the Oryzias latipes and O. sinensis fishes available in the NCBI GenBank.
Designation on Figure 2GenBank IDSpeciesLocalitySource
OS3F62HQ536423.1O. sinensisKorea[50]
OS1F128HQ536422.1O. sinensisKorea[50]
OSTaeanGU013788.1O. sinensisKorea: the Dongjin River[40]
OLSanghAP008948.1O. latipes (O. sinensis following Yoon et al., 2011)China: Shanghai[51]
OSLC09LC153109.1O. sinensisJapan: Aichi, Higashiyama ZooSuzuki-Matsubara M., Murase Y., Moriyama A., unpublished
OLFJ80FJ197680.1O. latipesnot specifiedPark J.-Y., An H.-S., Cho Y.-A., Kim K.-K., unpublished
OLSOKAP008947.1O. latipes (O. sinensis following Yoon et al., 2011)inbred strain, derived from eastern Korea [51]
OLKagaAP008940.1O. latipesJapan: Kaga[51]
OLKO94LC335803.1O. latipesJapan: Kanagava[52]
OLAminoAP008944.1O. latipesJapan: Amino[51]
OLHN1AB498066.1O. latipesJapan: HNI[53]
RO1MW695407O. sinensisRussia: Rostov provinceThis paper
RO1MW695408O. sinensisRussia: Krasnodar TerritoryThis paper
MBS2MW695409O. sinensisChina, TibetanAutonomous RegionThis paper

3. Results

According to our results, all sampled individuals of Oryzias from the Krasnodar Territory and the Rostov Region of Russia bear the same haplotype (Table 2), while Oryzias individuals collected in the Tibet Autonomous Region have another haplotype, differing by three nucleotide substitutions (Table 2; Figure 2). The median haplotype network (Figure 2) shows at least three well-defined groups of haplotypes. The haplotypes identified in the fish sampled in our study are part of a cluster formed by O. sinensis sequences. It should be specifically mentioned here that, although one of the haplotypes in this group, OLSangh, was listed in the GenBank (Genbank ID AP008948) as belonging to O. latipes, another study indicated that it belongs to O. sinensis [40]. Possibly, the haplotypes OLKaga and OLHN1 belong to the recently described species O. sakaizumii.
The morphological analysis revealed that the fish from the delta of the Don River (Rostov Region) have 8–10 (on average 8.5) rays in the pectoral fin. The fish from the Kuban River basin (Krasnodar Territory) have 8–9 (on average 8.75) rays, and those from the Yarlung Tsangpo basin (Tibetan Autonomous Region) have 9 rays. According to our results, the number of pectoral fin rays does not allow for the unambiguous taxonomic verification of O. sinensis. Within the examined fish samples, the highest variability of ray numbers was observed in the populations sampled from Russia, which reflects a previous report [35].

4. Discussion

According to genetic data, the fish that formed self-sustainable populations in two regions of the Russian Federation (the Rostov Region and the Krasnodar Territory), as well as in the Tibetan Autonomous Region of China, belong to the species Oryzias sinensis. According to earlier morphological studies, Oryzias fishes from Kazakhstan [21] and Ukraine [27] belong to the same species, but confirmation with molecular genetic methods is desirable.
The acquired data allow us to reconstruct the dispersal routes of O. sinensis across Eurasia with a high degree of certainty. It can be proposed that O. sinensis was transported to the Tibetan and Xinjiang Uyghur Autonomous Regions from eastern China. The exact timing of these introductions is unknown, but the genus Oryzias was not reported in Tibetan water bodies until the very end of the 20th century [54,55]. Its appearance in the mentioned region may have the same human-mediated vector as the appearance of another alien fish species, stone moroko (Pseudorasbora parva), in the same water body. The introduction of P. parva to the region is considered to be a result of the Buddhist religious practice of releasing live fish into water bodies [56]. However, an aquaculture-mediated cause cannot be ruled out. The appearance of O. sinensis in the Xinjiang Uyghur Autonomous Region is most likely explained by its unintentional introduction due to aquaculture vector, i.e., via the fishery supplementation of open waters by unverified stocking material.
From the Xinjiang Uyghur Autonomous Region, O. sinensis migrated to Kazakhstan via the Ili River, where numerous specimens of this species were recorded in October 1970 [57]. Subsequently, a total of 6200 Oryzias individuals were transported from this river to the Krasnodar Territory of Russia, and were released into six water bodies on 4 July 1974 for mosquito larval control [58]. It is proposed that the new population of Oryzias in Krasnodar expanded to water bodies in the Rostov Region (due to self-distribution along the hydrological network, and secondary unintentional translocations together with aquaculture stocking material), and further penetrated into southeastern Ukraine, where it was recorded in the Cis-Azov region on 15 June 2003 [27]. Oryzias fishes from Kazakhstan were also imported to Uzbekistan and Turkmenistan for mosquito control [24,59].
Thus, analysis of the Oryzias dispersal routes in continental Eurasia shows that O. sinensis, specifically, is expanding its range. An additional argument may be the fact that all reliably known routes of Oryzias dispersal in continental Eurasia began in China where O. sinensis is present, but O. latipes does not occur [32]. Non-native populations of O. latipes are only known to exist on the islands of the Japanese archipelago [28,43]. It is additionally noteworthy that the haplotype of the stone moroko found in Tibet is also present in native populations of this species inhabiting southeastern China [60]; so, it seems very likely that both the stone moroko and O. sinensis arrived to Tibet from southeastern China by the same vector and route.
In conclusion, it should be noted that we cannot exclude that the taxonomy of Oryzias is much more complex than presently assumed, and that OLSOK haplotype carriers, together with individuals with the OLFJ80 haplotype (GenBank ID FJ197680), belong to another, as-yet-undescribed species, since this group is separated from the compact cluster formed by O. sinensis by at least 77 nucleotide substitutions, which is about 12% of the sequence length studied (Figure 2). This markedly exceeds the typical level of interspecific variation in fishes (approximately 2% for the COI sequence, as suggested by Hebert et al. [42]).
The correct verification of species membership is not only important for identifying their dispersal routes, but also for determining the possible consequences of introducing an alien species into new ecosystems. For example, the invasiveness risk, an indicator that assesses the ability of a species to naturalize in a new region and change the native ecosystems, may be accurately calculated for certain species. The invasiveness risk of O. sinensis for the Brahmaputra River basin in the Tibetan Autonomous Region is assessed as moderately high [61].
A study of the expansion of O. sinensis suggests that it appears to be sufficiently tolerant to the cold, as it is able to naturalize in the water bodies of the Tibetan Plateau and the Rostov Region of Russia. Therefore, we cannot exclude the further expansion of new subranges of this species under global warming conditions in the Tibetan Plateau, southern Russia, and Ukraine, as well as penetration into India, downstream of the Brahmaputra River.

Author Contributions

All authors contributed to the conception and design of the study. Material preparation, data collection, and analysis were performed by A.A.M., V.S.A., Y.-H.S., Y.F., A.N.P. and A.N.R. The first draft of the manuscript was written by A.A.M., and all authors commented on previous versions of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

The processing of the material was supported by National Natural Science Foundation of China (or NSFC), no. 32011530077, and the manuscript was prepared with the support of Russian Science Foundation, project no. 21-14-00123.

Institutional Review Board Statement

The animal study protocol was approved by the Ethics Committee of the Severtsov Institute of Ecology and Evolution, the Russian Academy of Sciences (protocol #64).

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors are deeply grateful to Yu.Yu. Dgebuadze, B.I. Sheftel, and all members of the Institute of Zoology (China) and the Institute of Ecology and Evolution (Russia) expeditions for their help and assistance in the field work on the Tibetan Plateau, to A.S. Karyagina for providing valuable assistance during the expedition to the Kuban and Don River basins, to J.A. Titova for providing valuable comments on the manuscript, as well as to V.I. Petrashov for providing fish specimens from Chumyannyi Lagoon.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Map of Eurasia indicating the localities of ricefish (Oryzias) samples in the Rostov Region (A) and the Krasnodar Territory of the Russian Federation (B), as well as the Tibet Autonomous Region of China (C). Dark blue and light blue colors show the native and invaded ranges of the Chinese ricefish, Oryzias sinensis, respectively. Dark green and light green colors show the native and invaded ranges of the Japanese ricefish, O. latipes, respectively. Red arrows show probable translocations outside of the native range; black arrows show documented intentional secondary transportations. Wide open pink arrows show local short-distance translocations and self-distribution within river basins.
Figure 1. Map of Eurasia indicating the localities of ricefish (Oryzias) samples in the Rostov Region (A) and the Krasnodar Territory of the Russian Federation (B), as well as the Tibet Autonomous Region of China (C). Dark blue and light blue colors show the native and invaded ranges of the Chinese ricefish, Oryzias sinensis, respectively. Dark green and light green colors show the native and invaded ranges of the Japanese ricefish, O. latipes, respectively. Red arrows show probable translocations outside of the native range; black arrows show documented intentional secondary transportations. Wide open pink arrows show local short-distance translocations and self-distribution within river basins.
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Figure 2. Median haplotype network of the COI gene sequence for fishes belonging to the genus Ozyrias. See Table 2 for sample designations and descriptions. The numbers on the lines reflect the numbers of nucleotide substitutions.
Figure 2. Median haplotype network of the COI gene sequence for fishes belonging to the genus Ozyrias. See Table 2 for sample designations and descriptions. The numbers on the lines reflect the numbers of nucleotide substitutions.
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Table
Table 1. Sampling localities of fish (Oryzias sp.) with regards to information on regions: their coordinates (in geographical degrees); the number of measured fish individuals, N (the number of genotyped individuals is in parentheses); and their standard length SL, mm (means are in parentheses).
Table 1. Sampling localities of fish (Oryzias sp.) with regards to information on regions: their coordinates (in geographical degrees); the number of measured fish individuals, N (the number of genotyped individuals is in parentheses); and their standard length SL, mm (means are in parentheses).
LocalityCoordinatesDateNSL, mm
Rostov Region, Russia
(Don River basin)		N 47°5′43.2″;
E 39°19′1.5″		1.05.201910 (2)17.0–23.3 (19.8)
Krasnodar Territory, Russia
(Kuban River basin)		N 45°14′7.4″;
E 37°59′52″		11.05.20198 (2)18.5–25.5 (22.13)
Tibetan Autonomous Region, China
(Yarlung Tsangpo (Brahmaputra) basin)		N 29°21′24″;
E 90°42′55″		27.09.20121 (2)26
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Makhrov, A.A.; Artamonova, V.S.; Sun, Y.-H.; Fang, Y.; Pashkov, A.N.; Reshetnikov, A.N. New Records of the Alien Chinese Ricefish (Oryzias sinensis) and Its Dispersal History across Eurasia. Diversity 2023, 15, 317. https://doi.org/10.3390/d15030317

AMA Style

Makhrov AA, Artamonova VS, Sun Y-H, Fang Y, Pashkov AN, Reshetnikov AN. New Records of the Alien Chinese Ricefish (Oryzias sinensis) and Its Dispersal History across Eurasia. Diversity. 2023; 15(3):317. https://doi.org/10.3390/d15030317

Chicago/Turabian Style

Makhrov, Alexander A., Valentina S. Artamonova, Yue-Hua Sun, Yun Fang, Andrey N. Pashkov, and Andrey N. Reshetnikov. 2023. "New Records of the Alien Chinese Ricefish (Oryzias sinensis) and Its Dispersal History across Eurasia" Diversity 15, no. 3: 317. https://doi.org/10.3390/d15030317

APA Style

Makhrov, A. A., Artamonova, V. S., Sun, Y. -H., Fang, Y., Pashkov, A. N., & Reshetnikov, A. N. (2023). New Records of the Alien Chinese Ricefish (Oryzias sinensis) and Its Dispersal History across Eurasia. Diversity, 15(3), 317. https://doi.org/10.3390/d15030317

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