Introduction

The Chinese pond mussel, Sinanodonta woodiana (Lea, 1834) is a well-known invasive species of the Unionidae, which is widely spread almost around the world together with its alien fish hosts (Douda, Vrtílek, Slavík, & Reichard, 2012; Lajtner & Crnčan, 2011; Lopes-Lima et al., 2017; Watters, 1997). Recent molecular studies reveal that S. woodiana is rather a complex of several closely related species because it comprises at least seven deeply divergent mtDNA lineages (Bolotov et al., 2016). Among them, the two lineages could only be considered as invasive. The first one is the tropical invasive lineage, which is currently widespread across the Malay Peninsula, the Philippines, and through Indonesia to the Lesser Sunda Islands (Bolotov et al., 2016; Zieritz et al., 2016). The origin of this successful invader is uncertain, but several authors placed it within Taiwan or the southern regions of continental China based on the analysis of primary sources for introduced fishes (Bolotov et al., 2016; Djajasasmita, 1982; Watters, 1997). The second one is the temperate invasive lineage, which has broad nonnative range in Europe, but most likely originated from the Yangtze drainage basin (Bolotov et al., 2016; Watters, 1997).

S. woodiana may affect native mussel populations, including the negative impact via cross-resistance of host fishes (Donrovich et al., 2017; Sousa, Novais, Costa, & Strayer, 2014). Adult Sinanodonta mussels can compete effectively with indigenous taxa for space, food, and host fishes. Their ability to modify natural ecosystems influences biological, physical, and chemical parameters of water environment (Bolotov et al., 2016; Douda et al., 2012; Guarneri et al., 2014; Sousa, Gutiérrez & Aldridge, 2009, 2014; Watters, 1997). An infection of fishes with the glochidia of Sinanodonta may negatively affect their physiological conditions, size, and weight (Douda et al., 2017).

In the present correspondence, we report the first occurrence of S. woodiana from Myanmar. In addition, we discuss the possibility of the further spread of this lineage of S. woodiana species complex across river systems of Southeast Asia and its possible effects on the native freshwater communities.

Methods

Data Collection

Available cytochrome c oxidase subunit I (COI) sequences of S. woodiana species complex and its sister taxa were downloaded from the BOLD IDS and NCBI’s GenBank, resulting in 68 sequences from Europe, China, Russia, South Korea, Japan, Malaysia, the Philippines, and Indonesia (Table 1). The COI sequence, which was provided for the S. aff. woodiana specimen from Romania (NCBI’s GenBank acc. no. JQ435822), was not included (see Bolotov et al., 2016). We have analyzed three available specimens of S. woodiana, which were collected from a floodplain lake of the upstream section of the Irrawaddy River basin, Kachin State, Myanmar in November 2016 during the join fieldworks with specialists of Flora & Fauna International and Department of Fisheries of Myanmar (Table 1). In addition, six new samples of S. woodiana complex from Vietnam and Russia were also sequenced. Sequences of Margaritifera dahurica and M. laosensis were used as out-groups (GenBank acc. nos. KJ161530 and KR006699, respectively).

Table 1.

List of the Mitochondrial COI Sequences ofSinanodonta spp. Examined in the Present Study.

Results

A well-established population of S. aff. woodiana was discovered in a floodplain lake of the upstream section of the Irrawaddy River basin, Kachin State, Myanmar (Figures 1Figure 2. to 3). The mean shell length is 110.3 mm (90.2–128.5 mm, N = 20).

Figure 1.

Map of our new record (red asterisk) of the temperate invasive lineage of Sinanodonta aff. woodiana from Myanmar.

Figure 2.

Habitat of Sinanodonta aff. woodiana in Myanmar: A floodplain lake near Bhamo, the Irrawaddy River drainage basin, Kachin State, Myanmar.

Figure 3.

Shells of Sinanodonta aff. woodiana from a floodplain lake near Bhamo, the Irrawaddy River drainage basin, Kachin State, Myanmar: (a) Specimen no. RMBH biv269/15*, (b) Specimen no. RMBH biv269/16*, (c) Specimen no. RMBH biv269/9, and (d) Specimen no. RMBH biv269/6. An asterisk indicates sequenced specimens (Table 1). Scale bar = 2 cm.

The three sequenced specimens of S. aff. woodiana belong to a single COI haplotype, which is identical to that recorded from invasive populations in Europe and from native populations in China (Figure 4). This haplotype belongs to the temperate invasive lineage of Bolotov et al. (2016), which also comprises three additional haplotypes from China. The mean COI p-distance within the temperate invasive lineage varies from 0.15% to 0.66%.

Figure 4.

The majority-rule consensus phylogenetic tree of Sinanodonta spp. and sister taxa recovered from Bayesian inference analysis of an alignment comprising 33 unique COI haplotypes. In addition, haplotypes of Margaritifera dahurica and M. laosensis were used as out-groups (GenBank acc. nos. KJ161530 and KR006699, respectively). Numbers near nodes are Bayesian posterior probabilities. Haplotype codes and lineage codes correspond to Table 1. The scale bar indicates the branch length.

Populations from Malaysia, Indonesia, and Philippines belong to the tropical invasive lineage of Bolotov et al. (2016; see Figure 4). The sequenced specimens from Singapore are also representatives of this lineage, although they were obtained from ornamental trade (Ng et al., 2016). In contrast, the populations from Vietnam belong to a separate lineage that appears to be a native species, which inhabits the Red River basin (see Figure 4).

Discussion

Among countries of Southeast Asia, representatives of S. woodiana species complex were recorded from Malaysia, Indonesia, Singapore, Philippines, Cambodia, and Vietnam but were unknown from Myanmar, Thailand, and Laos (Bolotov et al., 2016; Ng et al., 2016; Zieritz et al., 2016, 2017).

Our sequenced specimens of S. woodiana from Irrawaddy basin surprisingly reveal the same COI haplotype that was recorded from invasive European populations and that belongs to the temperate lineage of Bolotov et al. (2016).

The taxonomy of S. woodiana species complex is unclear because it includes several divergent mtDNA lineages, each of which may represent a separate cryptic species (Bolotov et al., 2016; Froufe et al., 2017). Moreover, there is a plethora of nominal taxa that were synonymized with S. woodiana. With respect to an integrative approach (Konopleva, Bolotov, Vikhrev, Gofarov, & Kondakov, 2017), a taxonomic revision of such a species complex should be based on molecular sequence data obtained from the topotypes of each nominal taxon because old museum lots with dry shells are not appropriate for the extraction of high-quality DNA. The holotype of S. woodiana was collected from the Pearl River near Guangzhou (USNM: voucher no. 86380, the type locality: “Canton, China”), but any Sinanodonta sequences from this region, which may serve as reference sequences for the species, are not available.

Finally, the genus Sinanodonta should be a focus of the extensive taxonomic revision, along with efforts to estimate the distribution of invasive lineages and to detect the environmental threats and risks from alien mussel impacts.

Implications for Conservation

The actual distribution of S. woodiana in Myanmar is still unknown, although it seems to be rather local, because it was not recorded anywhere during our extensive fieldworks across the country (Bolotov et al., 2017a, 2017b). However, its possible spread through the country may affect native benthos communities, which include many unique endemic taxa of the Unionidae (Bolotov et al., 2017b). Our survey in the Bhamo area has shown that small lakes, which harbor the majority of mussel species in this region, may represent a suitable habitat for S. woodiana. The Chinese pond mussel could successfully inhabit these waterbodies and could compete with native mussels for resources and host fishes (Bolotov et al., 2016; Zieritz et al., 2016). Negative effects of the invasive S. woodiana on freshwater ecosystem functioning have been reported from Europe and Malaysia (Donrovich et al., 2017; Sousa et al., 2014; Zieritz et al., 2016). In Malaysia, this alien species replaced the native unionid assemblages in many river systems (Zieritz et al., 2016). However, we assume that further expansion of the temperate lineage across Southeast Asia may be limited due to the specific environment of tropical floodplain freshwater systems. These environmental conditions appear too warm for this cryptic taxon, which most likely originated from temperate China (see Figure 4). In contrast, a possible invasion of the tropical lineage into large freshwater basins of Myanmar (e.g., the Irrawaddy, Salween, and Sittaung drainage basins) seems to be much more dangerous because this lineage is adapted well to the environment of tropical monsoon freshwater systems, and it may therefore spread throughout the country.

Appearance of the Chinese pond mussel in Myanmar requires regular monitoring and other environmental measures from the government and conservation organizations. Dramatic declining of native species in Malaysia as a result of S. woodiana invasion is an example of lacking of special measures for the invasion management (Zieritz et al., 2016). We assume that current local range of S. woodiana in Myanmar provides benefits for invasion control and eradication efforts.