Molluscan Research

ISSN: 1323-5818 (Print) 1448-6067 (Online) Journal homepage: https://www.tandfonline.com/loi/tmos20

Salinity tolerance in different life history stages of an invasive false mussel sallei Recluz, 1849: implications for its restricted distribution

Suebpong Sa-Nguansil & Kringpaka Wangkulangkul

To cite this article: Suebpong Sa-Nguansil & Kringpaka Wangkulangkul (2020): Salinity tolerance in different life history stages of an invasive false mussel Mytilopsis￿sallei Recluz, 1849: implications for its restricted distribution, Molluscan Research, DOI: 10.1080/13235818.2020.1753902 To link to this article: https://doi.org/10.1080/13235818.2020.1753902

Published online: 20 Apr 2020.

Submit your article to this journal

Article views: 2

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tmos20 MOLLUSCAN RESEARCH https://doi.org/10.1080/13235818.2020.1753902

Salinity tolerance in different life history stages of an invasive false mussel Mytilopsis sallei Recluz, 1849: implications for its restricted distribution Suebpong Sa-Nguansila and Kringpaka Wangkulangkulb aDepartment of Biology, Faculty of Science, Thaksin University, Phatthalung, Thailand; bCoastal Ecology Lab, Department of Biology, Faculty of Science, Prince of Songkla University, Hat Yai, Thailand

ABSTRACT ARTICLE HISTORY Although the false mussel Mytilopsis sallei Recluz, 1849 is recognised as an aggressive invasive Received 12 June 2019 , its populations in several in Thailand are restricted to small areas. A salinity Final version received 3 April gradient is a major characteristic of its habitat, hence the effect of various salinity levels (0– 2020 40 ppt) on the mortality of larvae, juveniles and adults of M. sallei was investigated. ff KEYWORDS Condition Indices of adults reared at di erent salinity levels for two months were measured. Condition index; invasion; Spatial and temporal variations of salinity and false mussel abundance in a canal with a invasive species; larva salinity gradient were also monitored. After an acute (48 h) test, survival of larvae was highest at salinity levels of 12.5 and 16.25 ppt and decreased at lower and higher levels. Juveniles survived at all salinity levels, but most adults died in the first 24 h at a salinity of 40 ppt, while condition indices were lowest at salinity levels of 30 and 35 ppt. In the field survey, highest false mussel abundance was consistently found at the middle part of the canal with mid-range salinity. The results suggested that salinity is a determinant of survival in M. sallei larvae and potentially regulates the dispersal success of false mussels. However, the importance of salinity was marginal in the later stages of its life history.

Introduction Indo-Pacific region since the nineteenth century (Tan and Tay 2018). This false mussel exhibits high tolerance For aquatic species, not only land masses, but also to extreme and wide-ranging physical conditions, for unfavourable water quality conditions are dispersal example extreme salinity and petroleum hydrocarbon barriers that determine their biogeographic distri- contamination (Raju et al. 1975; Mohan and Prakash butions (Lockwood and Somero 2011; van der Gaag 1998). At locations where the false mussel is present et al. 2016). Salinity is one of the key environmental it usually dominates the local benthic communities. factors influencing survival, growth, activity and physi- At very high density its populations can change soft ology of marine organisms (Vernberg and Vernberg bottom into hard bottom habitat; as well as having 1972). Maintaining cell volume and normal physiologi- the potential to cause economic damage by destroying cal functioning in unfavourable salinity condition submerged man-made structures (Wangkulangkul and increases energy demand and also drives a reduction Lheknim 2008; Cai et al. 2014; Tan and Tay 2018). in their activity and energy acquisition (Berger and Although M. sallei is recognised as an aggressive Kharazova 1997). Knowledge of salinity tolerance, space occupier that has a potential to monopolise therefore, increases the understanding of marine infected areas and a wide distribution range might species’ dispersal and establishment capacities. be expected (Wangkulangkul and Lheknim 2008; Tan Several species of false mussels belonging to the and Tay 2018), many populations have restricted distri- family , for example the well-known butions, in that false mussels have never been found Dreissena polymorpha (Pallas, 1771), outside the areas where they were first observed quagga mussel Dreissena bugensis Andrusov, 1897, (Salgado-Barragán and Toledano-Granados 2006; Astu- and Conrad’s false mussel Mytilopsis leucophaeata dillo et al. 2014; Wells 2019). In Thailand, the establish- (Conrad, 1831), have been introduced and become ment of M. sallei populations was first reported from invasive in many countries on almost every continent estuaries and along the south of the Gulf of (Mackie and Schloesser 1996; Willan et al. 2000; Ther- Thailand in 2008 (Wangkulangkul and Lheknim 2008). riault et al. 2004). Mytilopsis sallei Recluz, 1849 is a In that report, the species was identified as Mytilopsis dreissenid, originally described from adamsi Morrison, 1946, however recent genetic analy- Guatemala and the Dominican Republic in the Bay of sis suggests that false mussels from the populations Mexico (Marelli and Gray 1983). It has invaded estu- established in Thailand belong to M. sallei (Wangku- aries, lagoons and marinas of many countries in the langkul and Klangnurak, in preparation). Recent

CONTACT Kringpaka Wangkulangkul [email protected] Coastal Ecology Lab, Department of Biology, Faculty of Science, Prince of Songkla University, Hat Yai 90110, Thailand © 2020 The Malacological Society of Australasia and the Society for the Study of Molluscan Diversity

Published online 20 Apr 2020 2 S. SA-NGUANSIL AND K. WANGKULANGKUL observations revealed that these populations do not phase, with hard mytiliform shells. Alien aquatic take over the entire estuaries or brackish parts of species anthropogenically introduced into a new lagoons, although the habitat seems suitable and habitat usually confront a sudden change in environ- there has been a considerable amount of time for mental conditions (van der Gaag et al. 2016). Moreover, them to disperse since they were first observed. Wang- abrupt increases and decreases in salinity in the kulangkul (2018) made a survey in the Songkhla Songkhla System have been recorded (per- Lagoon System, the largest coastal lagoon system in sonal observation). Therefore, standardised acute Thailand, and found that false mussel colonies were (48 h) tests on larvae, juveniles and adults of M. sallei present only within several of the rivers that are con- exposed to nine levels of salinity (0–40 ppt) following nected to the Thale Sap Songkhla Lake, the southern- ASTM (1999) were planned. Mussels were not acclimat- most part of the lagoon system, which is connected ised to lab conditions before conducting the tests. It to the sea. Interestingly, they were not found within was found in preliminary experiments (three rep- the lake itself. Hydrodynamics in the lake are governed etitions) that all planktonic larvae died after 48 h by freshwater discharges and tidal actions. Seasonal exposure to different salinities and the mortality rate fluctuation of salinity in this lake is substantial, could not be measured. We then decided to stop the ranging from freshwater to fully saline (Angsupanich experiment on planktonic larvae after 24 h exposure. and Kuwabara 1995; Wangkulangkul 2018). These The 48 h test on juveniles revealed that they tolerate physical attributes of the lake, especially salinity, may a very wide range of salinity (only one individual limit the migratory ability of the larvae which is the died, at 0 ppt), therefore the effects on adult mortality most vulnerable stage of bivalves (Bayne 1965; of long-term exposure (two months) to different sali- Verween et al. 2007). It was hypothesised that larvae nities were evaluated instead of conducting an acute or newly recruited false mussels are killed by high sal- test. Condition indices of adult M. sallei reared for two inity (∼35 ppt) in the lake during the dry season, months at different salinities were also measured. The restricting the mussels to rivers where salinity is gener- condition index (CI) relates the amount of shell to the ally lower (Wangkulangkul 2018). quantity of living tissue in bivalves. It has been used Experiments on the vulnerability of M. sallei to both in scientific research and commercial practice different salinities were conducted by Raju et al. (Davenport and Chen 1987). It is a useful indicator of (1975) and Nguyen and Tan (2011). They suggested the nutritional status and reflects the physiological that the false mussels exhibited a wide tolerance to performance of bivalves (Irisarri et al. 2015). In addition, different salinities including freshwater and hypersaline seasonal and spatial changes in salinity and M. sallei conditions (salinity 0–40 ppt). Trochophore and veliger abundance in a canal with a strong salinity larvae were observed in salinities ranging from 0 to gradient were monitored for over a year to examine 25 ppt (Raju et al. 1975). This provided baseline infor- the possible effect of this factor on the false mussels mation for understanding of the tolerance limits of in their habitat. false mussels. However the application of background information collected elsewhere for management of an invasive species might not be applicable to other Materials and methods ff ff locations because of the founder e ect (Simberlo Study site 2003; Sax et al. 2005). Moreover, in the study by Raju et al. (1975), only the presence/absence of false Surveys of false mussel distribution were carried out mussel larvae at different salinities was reported and monthly for 14 months from November 2017 to quantitative measurements were not conducted. Data December 2018 at the subtidal level at eight stations on the salinity tolerance of M. sallei larvae from other along Pawong canal in the Songkhla Lagoon System, locations are lacking (Wells 2019). As the preferred southern Thailand (Figure 1, 7°14′N, 100°34′E). All range of environmental conditions is usually narrower false mussel specimens used in experiments were col- than the tolerance limit range of a species (Verween lected by hand from patches found in Pawong canal. et al. 2007), the observations on the survival of the The canal is 5.5 km long and drains into the Thale false mussels in the short-term experiments of Raju Sap Songkhla Lake which is connected to the sea. A sal- et al. (1975) and Nguyen and Tan (2011) do not inity gradient is a major feature of this canal in which provide information on their optimal environmental salinity increases towards the mouth where it connects conditions. to the lake. Salinity is primarily influenced by rainfall, To investigate whether salinity is potentially one of runoff and tidal action and ranges from 0 to 33 ppt key determinants of M. sallei distribution, we tested (Angsupanich and Kuwabara 1999; Wangkulangkul the effects of salinity on the different life-history 2018). The main seasons in this region are the dry stages. The life cycle of M. sallei includes two important season (February–April) and the northeast monsoon phases: (1) a larval planktonic phase, during which indi- season (November–January); however, annual variation viduals are protected by soft shells, and (2) the benthic in the timing of these seasons has been recorded MOLLUSCAN RESEARCH 3

Figure 1. Pawong canal with 8 sampling stations (ST1–ST8). Generally, salinity decreases from ST1 to ST8. Inset: Location of the Songkhla Lagoon System in Thailand. Rectangle indicates the location of Pawong canal.

(Phasook and Sojisuporn 2005). The bottom of the Salinity tolerance of larvae canal is composed of various types of sediment, from Spawning induction and fertilisation pebbles and sandy loam to heavy clay. Mytilopsis sallei were found attached to hard sub- Collections for spawning induction were made in Feb- merged substrates, such as concrete poles and roots ruary 2019. Specimens were reared for three days in an of trees; as well as forming dense patches aquarium at 25°C and salinity of 5 ppt and were fed on the bottom of the canal. daily ad libitum with Chaetoceros sp. (3 × 105 cell/ml). Salinities were set up by using different concentrations of artificial salts (Aquarise©). Spawning induction and Survey of Mytilopsis sallei abundance fertilisation followed He et al. (2016). Three hundred Due to the high heterogeneity of the substrates to adults with a shell length of between 15 and 20 mm which the false mussels attach, assessment of density were selected. Epifaunal organisms were removed or actual percentage cover by this species was imprac- from shells by scrubbing and rinsing. False mussels tical. At each station, 2-dimensional percentage cover were exposed to air for 8 h and then placed in a 20 L of false mussels was visually evaluated within an area glass container filled with aerated artificial seawater of 2 × 2 m and separated into four categories: absent (5 ppt, 32°C). The salinity of solutions used in this pro- (0%), rare (<10%), common (10–80%) and abundant cedure was the same as the salinity of the natural (80–100%). In addition, the salinity in the immediate habitat where M. sallei were collected. Gonadal vicinity was measured using a hand-held extract was added to the container to induce - refractometer. ing. To obtain gonadal extract, gonads from 50 adults 4 S. SA-NGUANSIL AND K. WANGKULANGKUL were removed and ground in 300 ml of 20 µm filtered Salinity tolerance of juveniles seawater (5 ppt) and then filtered through a 100 µm Mytilopsis sallei matures at 8–10 mm shell length within mesh net. Eggs and sperm were released 6 h after a month (Karande and Menon 1975; Morton 1989); adding the extract. Around 0.5 h after spawning therefore, a single stage 48 h test was performed on adults were removed from the container then the sea- juveniles having 3–5 mm shell length. Specimens water was filtered through a 100 µm mesh net to were collected from the canal in March 2018. The mor- remove the remaining suspended matter, then tality rate of juveniles was assessed at 0, 5, 10, 15, 20, through 20 µm mesh net to remove excess sperm. 25, 30, 35 and 40 ppt. Each treatment consisted of This solution containing larvae was kept aerated in a three replicates. Twenty M. sallei were placed in a glass container. 300 ml plastic container and exposed to 200 ml of con- tinuously aerated test solution. The false mussels were fed once ad libitum with Chaetoceros sp. (3 × 105 cell/ Acute experimental test ml). All treatments were exposed to the same light con- M. sallei trochophore larvae develop into veligers (D- ditions and temperature (continuous lighting of two shaped) within 16 h after fertilisation (He et al. 2016). 10 W TL-light at 25°C). After 48 h, survivors were In this experiment 6 h old trochophore larvae were counted, and the percentage of mortality was exposed to different salinities for 24 h. At the end of calculated. the experiment all surviving larvae had developed into D-shaped larvae. The procedure used of Verween et al. (2007) was used. Salinities of test solutions were Salinity tolerance of adults 0, 5, 10, 15, 20, 25, 30, 35, and 40 ppt. Stock larvae sol- – ution (50 ml) was added to test solution (150 ml) of Adult false mussels of 10 15 mm shell length were col- each salinity in a plastic container to obtain a 200 ml lected from the canal in February 2019 and maintained solution. Therefore, the actual concentrations of the for two months at the same range of salinity used in the 200-ml solutions were 1.25, 5, 8.75, 12.5, 16.25, 20, larval survival experiments. Three replicates were con- 23.75, 27.5 and 31.25 ppt. Each level of salinity con- ducted. In each, 10 individuals were kept in a 5 L fi sisted of three replicates. All treatments were glass container lled with the test solution (prepared fi exposed to the same continuous lighting of two 10 W from arti cial salts). Temperature was kept constant TL-light. Temperature was kept constant at 25°C. The at 25°C. The test solution was continuously aerated larvae were not fed during the experiment and the and changed weekly. The false mussels were fed daily 5 test solutions were not aerated but the containers with an ad libitum diet of 3 × 10 cell/ml Chaetoceros were closed with lids to minimise evaporation. After sp. After two months, survivors were counted and the 24 h, the experiment was stopped by adding three CI of each was analysed. Shells were opened, then ml of 4% buffered formaldehyde and the larvae were tissue was removed, and the byssus was discarded. stained using Rose Bengal. Only larvae with filled The shells and tissue samples were oven dried at 60° shells were counted. Larvae were loaded into a 1 ml C for 48 h then dry mass (g) was measured to the Sedgewick-Rafter Counting Chamber and counted nearest 0.001 g using a digital weighing scale. CI was under a light microscope. The concentration of larvae calculated as [CI = tissue dry mass (g) × 100/dry shell (number of individuals per ml) of three weight (g)] (Davenport and Chen 1987). subsamples (one ml each) from each container was averaged to obtain the concentration of larvae in Data analysis each container. The exact concentration of larvae at the onset of the The Kruskal–Wallis test by ranks was performed to experiment in each container was not obtained by examine the effect of station (eight levels) and month counting before the experiment began because of (14 levels) on the abundance of M. sallei in the time-constraints given that the larvae would have Pawong canal. The effects of station and month on sal- developed into other stages when counting finished. inity were tested by two-way ANOVA without replica- Moreover, initial concentration could not be assumed tion. One-way ANOVAs were performed on the effect from total numbers of larvae (dead and alive) at the of salinity (a fixed factor, nine levels), on the density end of the experiment because dead larvae degraded of larvae and the percentage mortality of juveniles very quickly and would be difficult to identify. There- and adults. The percentage of juvenile mortality was fore, percentage of survival was not calculated but calculated as [% mortality = 100 × no. of dead individ- the initial concentration of larvae was assumed to be uals/20]. The percentage of adult mortality was calcu- similar across treatments and the difference in concen- lated as [% mortality = 100 × no. of dead mussels/10]. tration of surviving larvae between treatments at the Multiple comparisons of levels within significant end of the experiment was used to test the effect of factors were made using Student Newman Keuls different levels of salinity on larval survival. (SNK) tests. Cochran’s C test was performed to test MOLLUSCAN RESEARCH 5 for the heterogeneity of variance. Transformation was Salinity tolerance of false mussels carried out only where heterogeneity of variance was The highest survival of larvae was observed at salinities detected. The density of larvae was not transformed of 12.5 and 16.25 ppt (Figure 2A, Table 2). Survival while percentage mortality of adults was fourth root decreased in higher and lower salinities. No larva was (x + 1) transformed. Only one juvenile died during the found at salinity 31.25 and very few survived at salinity experiment (at 0 ppt). Zero mortality was recorded in 27.5, whereas at salinities 1.25 and 23.75 larval survival all other treatments. Cochran’s C test detected hetero- was less than half than that of the highest levels scedasticity of variance of transformed and raw data. (Figure 2A). Only one juvenile died during the 48 h To avoid the problems of heteroscedasticity and type experiment at 0 ppt. There was a difference in adult I error, statistical analysis was not performed on these mortalities between salinities (Figure 2C, Table 3). At data. Comparison of the CIs of falsemussels exposed a salinity of 40 ppt most individuals died within 24 h, to different salinities (fixed factor, nine levels) was per- and only three individuals in the total of 30 survived formed using univariate PERMANOVA with pairwise to the end of the two month experiment. The percen- comparison. Euclidean distance resemblance matrices tages of mortality did not differ between other sali- (with a dummy variable added) were constructed nities (Figure 2C, SNK). The CIs of adults were lowest from untransformed data (Anderson et al. 2008). The at 30–35 ppt; whereas the values were no different degrees of freedom differed among treatments between salinities 0–25, except that the CIs at 15 ppt because data were only obtained from survivors; there- differed from those at 20 ppt (Figure 2D, Table 4). The fore, PERMANOVA was used instead of the conven- CIs of three false mussels which survived after being tional ANOVA. At each level of salinity more than 20 kept at a salinity of 40 ppt were not different from false mussel specimens were used for CI analysis, the mussels exposed to other salinities (Figure 2D). except that at 40 ppt only three false mussels could be used. PERMDISP was performed to test the hom- ogeneity of multivariate dispersions (Anderson et al. Discussion 2008). The results of this analysis indicated that differ- ences in relative within-group dispersion among sali- The results from our experiments agree with previous nities (9 levels) were not statistically significant (F = studies: that the larval stage of a bivalve is the most

1.3042; df1 =8; df2 = 211; P(perm) = 0.40). Therefore, susceptible to physicochemical conditions (e.g. Qiu interpretation from the PERMANOVA analysis is argu- et al. 2002; Scanes et al. 2014), which is possibly due ably valid. to the lack of a protective shell (Verween et al. 2007). The Analysis ToolPak in Excel, Microsoft™ Office 365 The optimal range of salinity for M. sallei larvae to was employed for two-way ANOVA without replication survive was narrower than for juveniles and adults. while the Kruskal–Wallis test was carried out manually. The acute 24 h test clearly revealed that most larvae One-way ANOVAs were done using the GMAV5 survived at mid-level salinity, and that survival program. Multivariate analyses were performed in decreased towards both ends of the range of salinities PRIMER v7 add-on package PERMANOVA+ (Anderson tested. Juveniles and adults exhibited high tolerance et al. 2008). across salinities except that most adults died at the most extreme condition (salinity 40 ppt). It is important to note that the false mussels used in this experiment were not acclimatised. The sudden increase of salinity Results compared to very low where they were collected Survey of false mussel abundance (2 ppt) to the extreme level used in the experiment may have caused an osmotic shock leading to the The abundance of M. sallei in Pawong canal varied high mortality rate. across stations (Kruskal–Wallis test, K = 30.79; P < Long term exposure to high salinity reduced the 0.001) and months (Kruskal–Wallis test, K = 36.27; P condition indices of adults. However, if individuals sur- < 0.001). The effects of both factors on salinity were vived to the end of the experiment their condition was also significant (two-way ANOVA without replication, not worse than those of the false mussels exposed to station: F = 8.17, P < 0.001; month: F = 211.35, P < lower salinities. Tissue weight changes in dreissenids 0.001). The highest abundance of false mussels was are based upon nutritional state as well as gonadal found at stations located at the middle part of the development and release of gametes (Nalepa et al. canal (stations 4–6) with mid-range salinities and 2010). It is not possible in this experiment to distinguish the lowest abundance was usually found at station whether the low CI was a result of spawning or the 1 where the highest salinity was recorded in most poor conditions of the mussels in our study. Spawning of the months (Table 1). False mussels were recorded might occur as a response to increased environmental as abundant at salinities ranging from 0 to 26 ppt stress (Petes et al. 2007). Usually, mussels close their (Table 1). shells when exposed to unfavourable conditions, 6 S. SA-NGUANSIL AND K. WANGKULANGKUL

Table 1. Abundance of mussels and salinity levels (ppt) at 8 stations along Pawong canal from November 2017 to December 2018. Station Nov 17 Dec 17 Jan 18 Feb 18 Mar 18 Apr 18 May 18 Jun 18 Jul 18 Aug 18 Sep 18 Oct 18 Nov 18 Dec 18 1 ––––* * ** ** * * ––** 8 4 3 3 18 19 21 6 5 27 28 3 0 0 2 ––––* * ** *** ** *** ** ** ** ** 7 4 2 3 15 19 18 5 4 26 26 0 0 0 3 * * * ** *** *** ** *** *** *** *** *** *** *** 6 4 2 3 16 20 18 5 3 25 25 0 0 0 4 * ** ** ** *** *** *** *** *** *** *** *** *** *** 1 4 0 3 15 20 19 8 2 24 24 0 0 0 5 * ** ** *** *** *** *** *** *** *** *** ** ** *** 130392219822224000 6 * *** ** *** ** *** ** ** * *** *** ** *** *** 100382118822223000 7 –––* * *** ** *** ** *** *** ** ** ** 0 0 0 0 7 20 20 10 2 22 23 0 0 0 8**–––** * ** *** *** *** *** ** ** ** 000082015002018000 Remarks: Dash (–) = Absent; * = Rare; ** = Common; *** = Abundant. Notes: The distances from the mouth of the canal to station 7 and 8 are similar.

Figure 2. Mean (±SE) of A, Density of trochophore larvae at the end of 24 h experiment at different salinities; B, Percentage of juvenile mortality after 48 h test; C, Percentage of mortality; and D, condition Index of adult mussel after being exposed to different salinities for two months. while shell valve movement and clearance rate also Occurrence of M. sallei has been reported in a wide decrease (Raju et al. 1975; Curtis et al. 2000; Resgalla range of salinities in natural habitats. In Visakhapatnam, et al. 2007). Higher metabolic demand for maintaining India, they were observed at salinities of 15–35 ppt cell volume and avoiding osmotic shock in non-optimal (Raju et al. 1975). Wangkulangkul (2018) found salinity conditions (Berger and Kharazova 1997) along M. sallei in salinities of 0–35 ppt but most abundantly with the reductions of energy input from food can at levels between 0 and 23 ppt. The species was bring about the poor condition of the false mussels observed at localities in Singapore with salinity reared at high salinities. between 2 and 22 ppt (Tan and Morton 2006). Interest- ingly, M. sallei has been reported from several

Table 2. ANOVA testing for the effect of salinity on density of Table 3. ANOVA testing for the effect of salinity on percentage larvae. mortality of adults. Source of variance df SS MS FpSource of variance df SS MS Fp Salinity 8 6464.44 808.05 100.34 0.00* Salinity 8 3.68 0.46 4.59 0.003* Residuals 18 144.96 8.05 Residuals 18 1.80 0.10 Total 26 6609.41 Total 26 5.48 MOLLUSCAN RESEARCH 7

Table 4. PERMANOVA testing for the effect of salinity on the differ. Our study demonstrates salinity tolerance of condition indices of adult Mytilopsis sallei. M. sallei from a population in southern Thailand, but Source of variance df SS MS FPto understand environmental limits of other popu- Salinity 8 82.67 10.33 2.43 0.02* lations, we suggest that there is still a need for exper- Residuals 211 895.94 4.24 Total 219 978.61 iments to be carried out on specimens from the Note: Asterisks indicate significant effects. particular populations of interest. Future research should also investigate the response of M. sallei to other environmental factors, especially food avail- freshwater localities (Marelli and Gray 1983; Levings ability, pollutants and interactions with other species et al. 1994); however, the species has never been in the . Large-scale and long-term monitoring observed as a permanent resident in a fully freshwater of their abundance in other invaded estuaries will habitat, neither has it permanently colonised marine give more insight into variability of the environmental waters in Thailand (personal observation). In our limits of M. sallei and its adaptations to environmental study, at some stations the abundance of false changes. mussels varied greatly from absent to abundant within a few months. Salinity measured at the time of data collection may not reflect the optimal salinity Acknowledgements range for false mussels. Long-term monitoring of abun- This study was sponsored by Prince of Songkla University dance in a habitat with salinity gradient as performed (SCI601254S). We thank Wissarut Intararuang for production in our study may give more insight into favourable sal- of the map. We are grateful to Nutcha Buasakaew, Lutfee Haji- inity conditions of M. sallei. The facts that the overall wachi and Suphatsara Sangphuek for help during lab work. We thank the editor and reviewers for sharing their time highest abundance of M. sallei was found at the and knowledge to improve the manuscript. middle section of the canal and that the optimal sal- inity for survival of larvae was at mid-level, suggests that the favourable salinity range for establishment Disclosure statement – was brackish (salinity approximately 15 20 ppt) and No potential conflict of interest was reported by the author(s). narrower than the false mussel’s salinity tolerance limits. Not only environmental tolerance, but also the geo- Funding graphic spread of the favourable habitat, determines This work was supported by Prince of Songkla University: the invasion success of an introduced alien species [grant number SCI601254S]. (Verween et al. 2007). Estuaries are discrete and could be regarded as islands surrounded by fresh and sea- water. To colonise a new area, a brackish species References needs to cross these natural salinity barriers; therefore, Anderson, M., Gorley, R.N. & Clarke, R.K. (2008) Permanova+ it is less likely to disperse naturally compared to being for Primer: Guide to Software and Statistical Methods. transported by anthropogenic activity (Verween et al. Primer-E Limited, Ivybridge, Devon. 2007). We hypothesise that the restricted distribution Angsupanich, S. & Kuwabara, R. (1995) Macrobenthic fauna in Thale Sap Songkla, a brackish lake in southern Thailand. of M. sallei in the Songkhla Lagoon System and at Lakes & Reservoirs Research & Management 1, 115–125. other locations (e.g. Mexico in Salgado-Barragán and Angsupanich, S. & Kuwabara, R. (1999) Distribution of macro- Toledano-Granados 2006; Hong Kong in Astudillo benthic fauna in Phawong and U-Taphao canals flowing et al. 2014) is a result of recruitment failure where into a lagoonal lake, Songkhla, Thailand. Lakes & – larvae cannot cross salinity barriers. In Europe there is Reservoirs Research & Management 4, 1 13. ASTM (1999) Standard guide for conducting static acute tox- a wide distribution gap of Mytilopsis leucophaeata,an icity tests starting with embryos of four species of saltwater introduced brackish water species of North American molluscs. The American Society for Testing and Materials E origin, between the coasts of countries in western 724–798, 1–21. Europe and the (Verween et al. 2010; Zhuli- Astudillo, J.C., Wong, J.C.Y., Dumont, C.P., Bonebrake, T.C. & dov et al. 2015). Distribution of M. sallei in Thailand Leung, K.M.Y. (2014) Status of six non-native marine seems patchy, restricted to small areas of estuaries species in the coastal environment of Hong Kong, 30 years after their first record. BioInvasions Records 3, 123– and coastal lagoons (Wangkulangkul and Lheknim 137. 2008; personal observation). The establishment of dis- Bayne, B.L. (1965) Growth and the delay of metamorphosis of junct populations of M. leucophaeata and M. sallei at the larvae of Mytilus edulis (L.). Ophelia 2, 1–47. such localities might be a result of multiple introduc- Bayne, B.L. (1976) Marine Mussels: Their Ecology and Physiology tions by humans rather than natural dispersion, and (Vol. 10). Cambridge University Press, Cambridge. Berger, V.J. & Kharazova, A.D. (1997) Mechanisms of salinity links between populations may be weak or absent. adaptations in marine molluscs. In: Naumov, A.D., Moreover, the capability of disjunct populations to Hummel, H., Sukhotin, A.A. & Ryland, J.S. (Eds.), adapt to environmental circumstances may also Interactions and Adaptation Strategies of Marine 8 S. SA-NGUANSIL AND K. WANGKULANGKUL

Organisms: Proceedings of the 31st European Songkhla Lake Basin. Journal of Scientific Research Symposium, Held in St. Petersburg, Russia, 9–13 September Chulalongkorn University 4, 111–130. 1996, Springer Netherlands, Dordrecht, Netherlands, pp. Qiu, J., Tremblay, R. & Bourget, E. (2002) Ontogenetic changes 115–126. in hyposaline tolerance in the mussels Mytilus edulis and Cai, L.Z., Hwang, J.S., Dahms, H.U., Fu, S.J., Zhuo, Y. & Guo, T. M. trossulus: implications for distribution. Marine Ecology (2014)Effect of the invasive bivalve Mytilopsis sallei on Progress Series 228, 143–152. the macrofaunal fouling community and the environment Raju, P.R., Rao, K.M., Ganti, S.S. & Kalyanasundaram, N. (1975) of Yundang Lagoon, Xiamen, China. Hydrobiologia 741, Effect of extreme salinity conditions on the survival of 101–111. Mytilopsis sallei Recluz (Pelecypoda). Hydrobiologia 46, Curtis, T.M., Williamson, R. & Depledge, M.H. (2000) 199–206. Simultaneous, long-term monitoring of valve and cardiac Resgalla, C., De Souza Brasil, E. & Salomão, L.C. (2007) The activity in the blue mussel Mytilus edulis exposed to effect of temperature and salinity on the physiological copper. Marine Biology 136, 837–846. rates of the mussel Perna perna (Linnaeus 1758). Brazilian Davenport, J. & Chen, X. (1987) A comparison of methods for Archives of Biology and Technology 50, 543–556. the assessment of condition in the mussel (Mytilus edulis Salgado-Barragán, J. & Toledano-Granados, A. (2006) The false L.). Journal of Molluscan Studies 53, 293–297. mussel Mytilopsis adamsi Morrison, 1946 (: He, J., Qi, J.F., Feng, D.Q. & Ke, C.H. (2016) Embryonic and larval : Dreissenidae) in the Pacific waters of Mexico: A development of the invasive biofouler Mytilopsis sallei case of biological invasion. Hydrobiologia 563, 1–7. (Recluz, 1849) (Bivalvia: Dreissenidae). Journal of Sax, D.F., Stachowicz, J.J. & Gaines, S.D. (2005) Species Molluscan Studies 82, 23–30. Invasions: Insights into Ecology, Evolution and Irisarri, J., Fernández-Reiriz, M.J. & Labarta, U. (2015) Temporal Biogeography. Sinauer Associates Incorporated, and spatial variations in proximate composition and Sunderland. 495 p. Condition Index of mussels Mytilus galloprovincialis cul- Scanes, E., Parker, L.M., O’Connor, W.A. & Ross, P.M. (2014) tured in suspension in a shellfish farm. Aquaculture 435, Mixed effects of elevated pCO2 on fertilisation, larval and 207–216. juvenile development and adult responses in the mobile Karande, A.A. & Menon, K.B. (1975) Mytilopsis sallei, a fresh subtidal scallop Mimachlamys asperrima (Lamarck, 1819). immigrant in Indian harbours. Bulletin of the Department PLoS One 9, e93649. of Marine Sciences (Cochin University) 7, 455–466. Simberloff,D.(2003) How much information on population Levings, S.D., Garrity, S.D. & Burns, K.A. (1994) The Galeta oil biology is needed to manage introduced species? spill. III. Chronic reoiling, long-term toxicity of hydrocarbon Conservation Biology 17, 83–92. residues and effects on epibiota on mangrove fringes. Tan, K.S. & Morton, B. (2006) The invasive Caribbean bivalve Estuarine, Coastal and Shelf Science 38, 365–395. Mytilopsis sallei (Dreissenidae) introduced to Singapore Lockwood, B.L. & Somero, G.N. (2011) Invasive and native blue and Johor Bahru. Malaysia. The Raffles Bulletin of Zoology mussels (genus Mytilus) on the California coast: the role of 54(2), 429–434. physiology in a biological invasion. Journal of Experimental Tan, K.S. & Tay, T. (2018) The invasive Caribbean Mytilopsis Marine Biology and Ecology 400, 167–174. sallei (Bivalvia: Dreissenidae): a short review. ASEAN Mackie, G.L. & Schloesser, D.W. (1996) Comparative biology of Journal on Science and Technology for Development 35, zebra mussels in Europe and North America: an overview. 133–139. American Zoologist 36, 244–258. Therriault, T.W., Docker, M.F., Orlova, M.I., Heath, D.D. & Marelli, D.C. & Gray, S. (1983) Conchological redescriptions of MacIsaac, H.J. (2004) Molecular resolution of the family Mytilopsis sallei and Mytilopsis leucophaeata of the brackish Dreissenidae (Mollusca: Bivalvia) with emphasis on western Atlantic. Veliger 25, 185–193. Ponto-Caspian species, including first report of Mytilopsis Mohan, P.C. & Prakash, R.R. (1998) Concentration of pet- leucophaeata in the Black Sea basin. Molecular roleum hydrocarbons in bivalve Mytilopsis sallei and in Phylogenetics and Evolution 30, 479–489. the harbour waters of Visakhapatnam, east coast of India. van der Gaag, M., van der Velde, G., Wijnhoven, S. & Leuven, Indian Journal of Geo-Marine Sciences 27, 496–498. R.S.E.W. (2016) Salinity as a barrier for ship hull-related dis- Morton, B. (1989) Life-history characteristics and sexual strat- persal and invasiveness of dreissenid and mytilid bivalves. egy of Mytilopsis sallei (Bivalvia: Dreissenacea), introduced Marine Biology 163, 147. into Hong Kong. Journal of Zoology 219, 469–485. Vernberg, W.B. & Vernberg, F.J. (1972) Environmental Nalepa, T.F., Fanslow, D.L. & Pothoven, S.A. (2010) Recent Physiology of Marine . Springer-Verlag, New York. changes in density, , recruitment, size structure, Verween, A., Vincx, M. & Degraer, S. (2007) The effect of temp- and nutritional state of Dreissena populations in southern erature and salinity on the survival of Mytilopsis leuco- Lake Michigan. Journal of Great Lakes Research 36(Suppl. phaeata larvae (Mollusca. Bivalvia): the search for 3), 5–19. environmental limits. Journal of Experimental Marine Nguyen, T.K.D. & Tan, K.S. (2011) Biology of the Caribbean Biology and Ecology 348, 111–120. bivalve Mytilopsis sallei (Dreissenidae) in southeast Asia. Verween, A., Vincx, M. & Degraer, S. (2010) Mytilopsis leuco- In: Lutaenko, K.A. (Ed.), Proceedings of the Workshop phaeata: the brackish water equivalent of Dreissena poly- “Coastal Marine Biodiversity and Bioresources of Vietnam morpha? a review. In: van der Velde, G., Rajagopal, S., & and Adjacent Areas to the South China Sea”, Nha Trang, bij de Vaate, A. (Eds), The Zebra Mussel in Europe, Vietnam, November 24–25, 2011. Dalnauka, Vladivostok, Backhuys Publishers, Leiden, pp. 29–43. pp. 24–25. Wangkulangkul, K. (2018) Comments on restricted distri- Petes, L.E., Menge, B.A. & Murphy, G.D. (2007) Environmental bution of Mytilopsis adamsi Morrison, 1946, a non-native stress decreases survival, growth, and reproduction in New false mussel in the Songkhla Lagoon System, southern Zealand mussels. Journal of Experimental Marine Biology Thailand. 19, 151–156. and Ecology 351, 83–91. Wangkulangkul, K. & Lheknim, V. (2008) The occurrence of an Phasook, S. & Sojisuporn, P. (2005) Numerical model appli- invasive alien mussel Mytilopsis adamsi Morrison, 1946 cation on water circulation and salt dispersion in the (Bivalvia: Dreissenidae) in estuaries and lagoons of the MOLLUSCAN RESEARCH 9

lower south of the gulf of Thailand with comments on their 1849) (Bivalvia: Dreissenidae) in Australia. Molluscan establishment. Aquatic Invasions 3, 325–330. Research 20, 25–30. Wells, F.E. (2019) Environmental emergency: why did the false Zhulidov, A.V., Kozhara, A.V., van der Velde, G., Leuven, mussel Mytilopsis sallei not invade Darwin Harbour, R.S.E.W., Zhulidov, D.A., Gurtovaya, T.Y., Nalepa, T.F. & Australia? Malacologia 62, 247–256. Santiago-Fandino, V.J.R. (2015) New records from the Willan, R.C., Russell, B.C., Murfet, N.B., Moore, K.L., McEnnulty, Ponto-Azov region demonstrate the invasive potential of F.R., Horner, S.K., Hewitt, C.L., Dally, G.M., Campbell, M.L. & Mytilopsis leucophaeata (Conrad, 1831) (Bivalvia: Bourke, S.T. (2000) Outbreak of Mytilopsis sallei (Récluz, Dreissenidae). Journal of Molluscan Studies 81, 412–416.