BioInvasions Records (2019) Volume 8, Issue 2: 343–356

CORRECTED PROOF

Research Article strigata (Hanley, 1843) emerging as an invasive marine threat in Southeast Asia

Kitithorn Sanpanich1 and Fred E. Wells2,3,* 1Institute of Marine Science, Burapha University, 169 Longhadbangsaen Street, Tambon Saensuk, Amphur Moengchonburi, Chonburi Province 20131, 2School of Molecular and Life Sciences, Curtin University, GPO Box U1987, Perth, Western Australia 6845, Australia 3Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, Illinois 60605, USA Author e-mails: [email protected] (FEW), [email protected] (KS) *Corresponding author

Citation: Sanpanich K, Wells FE (2019) Mytella strigata (Hanley, 1843) emerging Abstract as an invasive marine threat in Southeast Asia. BioInvasions Records 8(2): 343–356, The Central and South American mytilid Mytella strigata was recently https://doi.org/10.3391/bir.2019.8.2.16 reported from the and Singapore, where its population has expanded exponentially in the last two years. We report the species has recently become Received: 22 November 2018 widespread in the inner Gulf of Thailand, with densities reaching 40,800m-2. It is a Accepted: 31 March 2019 potential threat to lucrative Asian green mussel ( viridis) aquaculture and Published: 2 May 2019 could be introduced to Australia, where it could foul pearl aquaculture farms. The Thematic editor: Cynthia McKenzie concurrent finding of the invasive false mussel Mytilopsis sallei at two new sites in Copyright: © Sanpanich and Wells Thailand emphasises the urgent requirement for a detailed invasive marine species This is an open access article distributed under terms survey in the region. of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0). Key words: invasive marine species, introduced marine pests, Thailand, Singapore, OPEN ACCESS. Philippines, Mytilopsis sallei

Introduction There is an increasing awareness of the risk invasive marine species (IMS, also known as introduced marine pests) pose to marine environments. IMS can dominate their new environment, change ecosystems, outcompete native species, threaten fisheries and aquaculture, introduce diseases and interfere with industrial facilities (Johnson and Chapman 2007; Molnar et al. 2008; Wells et al. 2009; Crowe and Frid 2015). The adverse effects of a newly established IMS may rapidly become apparent or it can take decades before they can be detected. For example, the Red Sea mytilid pharaonis (P. Fisher, 1870) moved through the Suez Canal into the eastern Mediterranean shortly after the canal was opened in 1869. It was first reported from Port Said in 1875, but it was a hundred years later that B. pharaonis was reported as invasive. It is now widely distributed in the eastern Mediterranean (Rilov et al. 2004; Dogan et al. 2007). Several species have invaded tropical marine environments after moving from one marine biogeographic region to another. The best recent examples are the Pacific lionfish Pterois volitans (Linnaeus, 1758) and P. miles

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 343 Mytella strigata in Southeast Asia

(Bennett, 1828) which were introduced to Florida in the 1990s. Both are now widespread in the , where they compete with and prey on native species, substantially altering local ecosystems (Albins and Hixon 2008). A study of 71 reefs demonstrated that the effect of lionfish was independent of the density of native predatory fish (Hackerott et al. 2013). Recruitment of native coral reef fishes declined by 79% following the introduction of P. volitans (Albins and Hixon 2008), with populations of small native fish decreasing 95% at some sites (Côté et al. 2013). In a second example, the Asian green mussel (Linnaeus, 1758) was first recorded in Trinidad, West Indies in 1990 (Agard et al. 1992). It is now widespread in the Caribbean and has reached Florida and Georgia, USA (Buddo et al. 2003; SCAISTF 2007). Perna viridis has a higher fecundity than the native mussel Brachidontes exustus (Linnaeus, 1758) and the virginica (Gmelin, 1791) raising concern that it might outcompete these species (Barber et al. 2005; McFarland et al. 2014). The green mussel also fouls cooling systems, navigation buoys, floating docks, piers and pilings. It accumulates toxins and can cause paralytic poisoning (NIMPIS 2017). Thirdly, the Caribbean Sea false mussel Mytilopsis sallei (Récluz, 1849) has become invasive in a wide range of Asian countries, including (Kalyanasundaram 1975; Morton 1981), Singapore and Malaysia (Tan and Morton 2008), Taiwan (Chang 1985), Hong Kong (Morton 1980; Huang and Morton 1983), China (Cai et al. 2014) and Japan (Habe 1980; Furuse and Hasegawa 1984). The species invaded Darwin, Australia in 1999, but was successfully eliminated (Willan et al. 2000). It has also invaded Thailand where it is referred to as the eastern Pacific M. adamsi (Morrison, 1946) (Wangkulangkul and Lkheknim 2008; Wangkulangkul 2018). The mytilid Mytella strigata (Hanley, 1843) (previously known as M. charruana (d’Orbigny, 1842)) is native to both coasts of Central and (Lim et al. 2018). It has recently become invasive in Florida and Georgia (Boudreaux and Walters 2006; Gillis et al. 2009). Chavanich et al. (2010) provided a detailed analysis by country of introduced marine species in Southeast Asia, but M. strigata was not known in the region. However, it has since been reported from both the Philippines (Rice et al. 2016; Mediodia et al. 2017; Vallejo et al. 2017) and Singapore (Lim et al. 2018). In October 2017 the senior author was contacted about an unidentified mussel being found in Samut Prakan Province, Thailand that was causing concern among local P. viridis growers. We report here that the mussel is M. strigata. It is now widespread and invasive in the inner Gulf of Thailand. We are concerned that M. strigata will cause considerable disruption to the P. viridis fishery and marine ecosystems in Southeast Asia.

Materials and methods A brief survey was made of the site from which the were reported in April 2018 and a more detailed survey of the inner Gulf of Thailand was

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 344 Mytella strigata in Southeast Asia

Figure 1. Locations surveyed in the inner Gulf of Thailand. 1 Prachuap Kiri Khan Coastal Aquaculture Research and Development Center, Klongwarn. 2 Sirinart Rajini Mangrove Ecology Learning Center. 3 Cha Am. 4 Puktiem Beach. 5 Ban Kunsai. 6 Coastal Aquaculture Research and Development Center, Samut Sakhon Province. 7 Prawn farm, Tumbon Puntainorasing, Amphur Moeng, Samutsakorn Province. 8 Khumsamutjin Temple, Tumbon Laemphapa, Amphur Prasamutjedi, Samutprakarn Province. 9 Bangpakong River mouth, Chonburi Province. 10 Offshore of Bangpakong River mouth, Chonburi Province. 11 Bangpakong River mouth, Chonburi Province. 12 Sriracha Fisheries Research Station. BP Bangkok port. LC Laem Chabang port. For details see Supplementary material Table S1.

conducted in November 2018 (Figure 1, Supplementary material Table S1). The site at Samut Sakhon is fringed with small (< 3 m high) mangroves. The margins of the aquaculture ponds of both Prachuap Khiri Khan and Samut Sakhon are carpets of M. strigata several centimetres thick in soft mud. Clumps of mussels were pulled from the bottom by hand and placed flat on a sample tray. A 50 × 50 cm quadrat with monofilament line marking every 10 cm was placed over each clump and a 10 × 10 cm sample was cut out of the clump. Eight samples were taken from each site. The clump was broken up, then the mussels were, washed, identified and measured with callipers. Salinity was measured with a hand held Atago Manual salinometer.

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 345 Mytella strigata in Southeast Asia

Figure 2. The prawn farm at Prachuap Kiri Khan where Mytella strigata were first detected in the inner Gulf of Thailand in November 2017. Photo credit: Kitithorn Sanpanich.

A survey was made by road between Prachuap Khiri Khan and Samut Sakhon. Several sites along the road were inspected for M. strigata (Table S1, Figure 1), but no additional mussels were found. Two sites were surveyed by boat at the mouth of the Bangpakong River and a third location just offshore. At each site a bamboo pole that had been driven into the mud was removed. No mussels were found on the poles at the river mouth, but the pole from the open water of a P. viridis farm was heavily fouled. Five 30 cm lengths were cut from the pole at approximately equal distances. The clumps of biofouling, which was primarily large individuals of P. viridis heavily overgrown by barnacles, was broken up. The mussels were cleaned, identified, counted and measured. The final survey site was a small P. viridis research farm operated by Kasetsart University at Si Racha, Chonburi Province. Several of hanging ropes were removed from the water and inspected for M. strigata.

Results Mytella strigata were introduced into the aquaculture farm at Prachuap Khiri Khan from Samut Sakhon in November 2017 to trial as fish food. This was unsuccessful and the mussels are now being used as food for spiny lobsters. A size frequency analysis of 300 individuals collected in April 2018 ranged 30 to 61 mm in length with a mean of 48.6 ± 0.3 mm (SE) (Table S1, Figures 1 to 4). The November 2018 survey was made a year after M. strigata were introduced to the pond. By then the mussels had spread to at least one adjacent pond. A total of 3264 M. strigata were collected

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 346 Mytella strigata in Southeast Asia

Figure 3. Shells of Mytella strigata collected at Prachuap Kiri Khan in April 2018. Photo credit: Kitithorn Sanpanich.

Figure 4. A clump of Mytella strigata from the pond at Prachuap Kiri Khan in November 2018. Photo credit: Kitithorn Sanpanich.

in eight quadrats at Prachuap Khiri Khan, giving a mean density of 40,800 ± 2565 m-2 (SE). Measurement of 1219 individuals showed that the population was bimodal (Figure 5). Seventeen adults ranged in size from 38 to 51 mm, with a mean of 43.5 ± 0.8 mm. The bulk of the population was 1202 juveniles that ranged from 4 to 20 mm, with a mean of 13.3 ± 0.1 mm (SE).

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 347 Mytella strigata in Southeast Asia

Figure 5. Size frequency graphs of Mytella strigata and Perna viridis from the inner Gulf of Thailand.

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 348 Mytella strigata in Southeast Asia

Figure 6. Biofouling, including Perna viridis and Mytella strigata, on the bamboo pole from offshore of the Bangpakong River. Photo credit: Kitithorn Sanpanich.

There were also 536 M. sallei in seven samples analysed at Prachuap Khiri Khan in November 2018, giving a mean density of 7657 ± 1662 m-2 (SE). Measurement of 426 individuals showed they were 4 to 20 mm long, with a mean of 11.0 ± 0.1 mm (SE). A total of 521 M. strigata were collected in the eight quadrats at Samut Sakhon in November 2018, giving a mean density of 6512 ± 1082 m-2 (SE). The mean size was 34.5 ± 0.5 mm, with a range of 13 to 60 mm (Figure 5). A total of 57 paired valves of Mytilopsis sallei were found in the samples, but most were dead. The M. sallei were all overgrown by M. strigata, suggesting that they had been outcompeted. Both M. strigata and P. viridis were found in all five lengths of the bamboo pole from Bangpakong, so they inhabit the full depth of the water column from the bottom to the surface. The diameter of the pole was 3 cm; biofouling was up to 24 cm wide (Figure 6). A total of 1199 M. strigata were collected for a mean density of 239.8 ± 81.1/30 cm (SE). The mussels ranged in size from 7 to 36 mm with a mean of 19.1 ± 0.2 mm (SE) (Figure 5). In addition, 421 P. viridis were collected, giving a mean of 84.2 ± 8.9/30 cm (SE) (Figure 5). The population of P. viridis was bimodal. Most (391) were large individuals that ranged from 23 to 80 mm with a mean of 50.24 ± 0.49 mm (SE). Twenty-nine small individuals were 6 to 13 mm long, with a mean of 8.7 ± 0.9 mm (SE) (Figure 5). The Sriracha site is between the extensive port facilities at Laem Chabang < 10 km to the south and commercial P. viridis farms immediately to the north. The survey on 14 November 2018 found small individuals of M. strigata mixed in with the P. viridis.

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 349 Mytella strigata in Southeast Asia

Figure 7. Mytella strigata being sold in the market in Puntainorasing, Samutsakorn Province in June 2018. Photo credit: Kitithorn Sanpanich.

Mytella strigata were being sold in the local market at Phanthai Norasing in Samut Sakhon Province in June 2018 (Figure 7). The price of 35 to 50 Thai baht (approximately 1.00 to 1.40 USD) is similar to P. viridis of the same size. The farmer reported that this species grows rapidly and competes for with the native Perna viridis. When some of the invasive mussels died, they covered the bottom of the prawn farm pond causing oxygen deprivation and the prawns died. No mussels were being sold in the markets in November 2018. Both fishermen and market stall holders indicated in November that this was not the season for M. strigata.

Discussion Mytella strigata was first found in the Philippines in 2014 (Rice et al. 2016; Mediodia et al. 2017; Vallejo et al. 2017) and in Singapore in March 2016 (Lim et al. 2018). Genetic analysis of both populations suggests they originated from the Caribbean coast of South America (Rice et al. 2016; Lim et al. 2018). Lim et al. (2018) reported that three specimens in the Cuming Collection of the Natural History Museum, London from the 1840s have a locality label of the Philippines. They suggested a possibility that M. strigata may have been introduced to the Philippines centuries ago by Spanish galleons travelling from South America to Spain then undertaking a separate voyage to the Philippines. The M. strigata populations would then have remained undetected until 2014. Such populations could have been the source of the Singapore introduction. Alternatively, Lim et al. (2018) state that the Philippines locality in the Cuming Collection may be

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 350 Mytella strigata in Southeast Asia

incorrect. This is much more likely. Given the very recent detection of M. strigata in both the Philippines and Singapore, M. strigata was probably introduced to Thailand from a native population in the Americas, either in ballast water or biofouling, as most IMS are distributed by vessels (Keller et al. 2010; Seebens et al. 2013). Sanpanich (2011) undertook a detailed analysis of bivalves occurring at 55 stations in eastern Thailand, including 20 in Chonburi Province where the sites at the Bangpakong River and Sriracha are located. A total of 321 species were recorded, but M. strigata was not found. Additional sampling in eastern Thailand since then did not detect the species until it was reported in from Prachuap Khiri Khan in November 1997 (Sanpanich, unpublished). Similarly, Chavanich et al. (2010) did not list the species in their survey of introduced species in Southeast Asia. While we do not know when M. strigata was introduced to the inner Gulf of Thailand, it must have been very recently. Mature specimens were present Prachuap Khiri Khan at least as long ago as November 2017. The finding of M. strigata in high densities at four widespread sites demonstrates that the mussel is well established across the inner Gulf of Thailand. Lim et al. (2018) found the species in both artificial and natural in Singapore. To date it has only been found in aquaculture sites in Thailand, but two of the P. viridis sites were in open water. The November 2018 survey was conducted at a time of year when there are no daytime low tides in the area, so we do not yet know whether populations are already present in natural intertidal habitats. Stenyakina et al. (2010) reported that M. strigata matures at a length of only 1.25 cm. The size-frequency data Prachuap Khiri Khan, with a mean of 48.3 mm and a maximum size of 61 mm in April 2018, demonstrates that the population was composed of adults at the time. By November the population at Prachuap Khiri Khan was bimodal, with almost all individuals being young juveniles with an average length 13.3 mm. There was a residual population of adults that averaged 43.5 mm. The presence of M. strigata in the inner Gulf of Thailand is of particular concern as the two largest ports in Thailand are in the area where it was detected. Laem Chabang Port (Figure 1) is the larger, handling 13,313 vessels in 2017. There are also extensive support facilities such as drydocks and a floating drydock (LCP 2018). Bangkok Port, the second largest port, is also on the inner Gulf of Thailand (Figure 1). In fiscal year 2016 Bangkok Port handled 3,067 vessels with 21 million tonnes of cargo (Wikipedia 2018). The two ports provide ready transport mechanism for M. strigata into the inner Gulf of Thailand. Now that M. strigata is established in the region, they also serve as a source of M. strigata for distribution widely in Thailand and other countries. Lim et al. (2018) suggest the are probably more populations of M. strigata in Southeast Asia that have not yet been detected. The subsequent finding of M. strigata in the inner Gulf of

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 351 Mytella strigata in Southeast Asia

Thailand confirms this suggestion. Kantavong (pers. comm.) reported that commercial aquaculture of P. viridis occurs on the Andaman Sea coastline of Thailand. While P. viridis occurs there, it is not common, and young mussels are shipped to Phuket for grow-out. This raises the possibility that M. strigata can be inadvertently introduced to Phuket. A number of species of mytilid mussels are important aquaculture species. Mytilids typically have a high fecundity, rapid growth rate, are filter feeders and are tolerant of a wide range of environmental conditions, all attributes that make them ideal for aquaculture. However, these features also make them potential . Mytella strigata clearly fits into this category. It is tolerant of a wide range of salinities, between 2 and 40 psu (Yuan et al. 2010; Rice et al. 2016) and is a common constituent of biofouling (Kauano et al. 2017). The wide salinity tolerance of the species was reflected in the inner Gulf of Thailand, where populations were found in salinities ranging from 7 to 35 ppt. The Asian green mussel Perna viridis dominates Asian mussel aquaculture, with production varying from about 150,000 to 300,000 tonnes annually since 2000 (FAO 2018). The suggestion by fishers and stall holders in Thailand that M. strigata competes with P. viridis is a particular concern. Rice et al. (2016) considered the two have different seasonal growth patterns in the Philippines and might complement each other as aquaculture species. The fact that M. strigata are being sold in Thai markets suggests there is currently a minor economic benefit to the species. They have also been trialled as a potential food supply for rock lobsters (Phumthong, pers. comm.). In having a dual role as an economic benefit while at the same time being an IMS, M. strigata in Thailand would parallel the situation with the gigas (Thunberg, 1793) in southern Australia. The Pacific oyster was introduced into Tasmania in 1949 as a potential aquaculture species (Thomson 1952, 1959). It has been very successfully cultivated and now supports an industry worth millions of dollars annually. However, the species has spread widely in southeastern Australia and there are feral populations that have caused the species to be classified as an IMS (NIMPCG 2010a, b). In contrast to Rice et al. (2016), Lim et al. (2018) found M. strigata may possible outcompete P. viridis. Asian green mussels monitored on plastic sheeting in Singapore had recruitment peaks in December 2014 and 2015, before the arrival of M. strigata. There was no such peak in December 2016, after the arrival of M. strigata. Lim et al. (2018) reported densities of M. strigata exceeding 10,000 individuals in 100cm-2 and it is spreading rapidly. The potential for a M. strigata to outcompete the lucrative P. viridis is a serious concern that urgently needs to be assessed. Branch and Steffani (2004) investigated the spread of the mussel Mytilus galloprovincialis Lamarck, 1819 in South . The species arrived in the mid1970s and by the time of their report had become widespread in South

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 352 Mytella strigata in Southeast Asia

Africa, outcompeting several local species. Branch and Steffani (2004) attributed the success of M. galloprovincialis to several factors, including high productivity, predominately strong wave action, lack of predators and parasites, and the mussel’s fast growth rate, high fecundity and planktotrophic larval stage. The last three biological features are characteristic of mytilids. The explosion of the population of M. strigata in the aquaculture pond at Prachuap Khiri Khan demonstrates both its high fecundity and rapid growth rate. TWAP (2018) shows that the Gulf of Thailand has a high primary productivity, and productivity in the aquaculture farms would be expected to be higher as nutrients are artificially added. While no data are presented on predators in the P. viridis farms in open waters in the inner Gulf, there would be little or no predation of the mussels in the aquaculture ponds. The net result has been a rapid increase in populations of M. strigata in the inner Gulf of Thailand. Perna viridis in Chonburi are cultivated in two ways: on bamboo poles anchored in the sea floor and extending above the water surface and on ropes hanging down from floats on the sea surface. The bamboo poles remain intact for only one year, so the mussels must be harvested at a relatively small size. Mussels are retained on the hanging ropes for two to three years, allowing continuous harvesting at greater sizes (Kantavong, pers. comm.). This harvesting method means that there would be no possibility of separate seasonal harvesting of M. strigata and would increase the period during which M. strigata could compete with P. viridis. Australia has a strong biosecurity program to prevent marine pest species from being introduced to the country (NIMPCG 2010a, b). However, there is considerable vessel movement between Southeast Asia and Australia. For example, Bridgwood and McDonald (2014) undertook a detailed survey of the risks of marine pest introductions to all of the major Western Australian ports. Vessel arrivals were reported from Singapore, Philippines and Thailand, with Singapore having the most vessels. If M. strigata is introduced into WA it could foul Pinctada maxima (Jameson, 1901) aquaculture sites. This is the most valuable aquaculture species in WA, a value of $ 71 million Australian in 2017 (Hart et al. 2018). As described above, the initial detection of M. strigata in the inner Gulf of Thailand was accidental. Four populations were found in a brief survey and the species is well established. There is an urgent need for a more detailed survey to determine the extent of the M. strigata populations in the region. Similarly, the Caribbean black striped mussel Mytilopsis sallei is well known to be established in Songkla Lake in southern Thailand, where it was reported as M. adamsi (Wangkulangkul and Lkheknim 2008; Wangkulangkul 2018). The presence of two IMS mollusc species in different parts of the country raises the more important requirement for a broader survey of potential IMS species in Thailand.

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 353 Mytella strigata in Southeast Asia

Acknowledgements

We gratefully acknowledge the support of Mr. Tanet Phumthong, Director of the Prachuap Khiri Khan Coastal Aquaculture Research and Development Center (Klongwarn) who made the initial report of the unidentified bivalve. Dr Tan Koh Siang of the National University of Singapore identified it as M. strigata. Mr Teerapong Duangdee of Kasetsart University, Bangkok participated in the June field survey. For the November survey we acknowledge Ms. Napaphach Luangkhamin and other staff of the Marine and Coastal Resources Research Center Upper Gulf of Thailand, Mr. Attawut Kantavong, Sriracha Fisheries Research Station, Faculty of Fisheries, Kasetsart University and Mr Pricha Suwan, skipper of the vessel Tipsuwan. This work was partially supported by the National Research Council of Thailand project: The study on the status of marine bivalves, Family : alien species along Thailand coast (budget year 2016). Figure 2 was modified from https://www.thairath.co.th/content/777557. We are pleased to acknowledge the assistance of the manuscript reviewers.

References

Agard J, Kishore R, Bayne B (1992) Perna viridis (Linnaeus, 1758): first record of the Indo- Pacific green mussel (: ) in the Caribbean. Caribbean Marine Studies 3: 59–60 Albins MA, Hixon MA (2008) Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Marine Ecology Progress Series 367: 233–238, https://doi.org/ 10.3354/meps07620 Barber BJ, Fajans JS, Baker SM, Baker P (2005) Gametogenesis in the non-native green mussel, Perna viridis, and the native scorched mussel, Brachidontes exustus, in Tampa Bay, Florida. Journal of Shellfish Research 24: 1087–1095, https://doi.org/10.2983/0730-8000(2005) 24[1087:gitngm]2.0.co;2 Boudreaux ML, Walters LJ (2006) Mytella charruana (Bivalvia: Mytilidae): a new, invasive bivalve in Mosquito Lagoon, Florida. The 120: 34–36 Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case-study of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). Journal of Experimental Marine Biology and Ecology 300: 189–215, https://doi.org/10.1016/j.jembe.2003.12.007 Bridgwood S, McDonald J (2014) A likelihood analysis of the introduction of marine pests to Western Australian ports via commercial vessels. Department of Fisheries, Western Australia, Fisheries Research Report 259: 1–212 Buddo DSA, Steele RD, D’Oyen ER (2003) Distributions of the invasive Indo-Pacific green mussel, Perna viridis, in Kingston Harbour, Jamaica. Bulletin of Marine Science 73: 433– 441, https://doi.org/10.3391/bir.2012.1.3.03 Cai L-Z, Hwang J-S, Dahms H-U, Fu S-J, Guo T (2014) Effect of the invasive bivalve Mytilopsis sallei on the macrofaunal fouling community and the environment of Yundang Lagoon, Xiamen, China. Hydrobiologia 741: 101–111, https://doi.org/10.1007/s10750-014-2012-4 Chang KM (1985) Newly introduced false mussel to Taiwan (Bivalvia: Dreissenidae). Bulletin of Malacology, ROC 11: 61–67 Chavanich S, Tan LT, Vallejo B (2010) Report on the Current Status of Marine Non-Indigenous Species in the Western Pacific Region. Chulalongkorn University, Bangkok, 71 pp Côté IM, Green SJ, Hixon MA (2013) Predatory fish invaders: insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biological Conservation 164: 50–61, https://doi.org/10.1016/j.biocon.2013.04.014 Crowe TP, Frid CLJ (2015) Marine Ecosystems. Human Impacts on Biodiversity, Functioning and Services. Cambridge University Press, Cambridge UK, 406 pages, https://doi.org/10.1017/ cbo9781139794763 Dogan A, Önen M, Öztürk B (2007) A new record of the invasive Red Sea mussel (Fischer P., 1870) (Bivalvia: Mytilidae) from the Turkish coasts. Aquatic Invasions 2: 461–463, https://doi.org/10.3391/ai.2007.2.4.20 FAO (2018) Cultured Aquatic Species Information Programme Perna viridis (Linnaeus, 1758). Fisheries and Aquaculture Department, Food and Agriculture Organization of the United Nations. http://www.fao.org/fishery/culturedspecies/Mytilus_edulis/en (accessed 19 September 2018) Furuse K, Hasegawa K (1984) Mytilopsis sallei found in Tokyo Bay. Chiribotan 15: 18 Gillis NK, Walters LJ, Fernandes FC, Hoffman EA (2009) Higher genetic diversity in introduced than in native populations of the mussel Mytella charruana: evidence of population admixture at introduction sites. Diversity and Distributions 15: 784–795, https://doi.org/10.1111/j.1472-4642.2009.00591.x Habe T (1980) Mytilopsis sallei (Récluz, 1849), a newly introduced mussel to Japan. Chiribotan 11: 41–42 Hackerott S, Valdivia A, Green SJ, Côté IM, Cox CE, Akins L, Layman CA, Precht WF, Bruno JF (2013) Native predators do not influence invasion success of Pacific lionfish on Caribbean reefs. PLoS ONE 8: e68259, https://doi.org/10.1371/journal.pone.0068259

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 354 Mytella strigata in Southeast Asia

Hart A, Murphy D, Jones R (2018) Pearl oyster managed fishery resource status report 2017. In: Gaughan DJ, Santoro K (eds), Status Reports of the Fisheries and Aquatic Resources of Western Australia 2016/17: The State of the Fisheries. Department of Primary Industries and Regional Development, Western Australia, pp 138–141 Huang ZG, Morton B (1983) Mytilopsis sallei (Mollusca: Dreissenoidea) established in Victoria Harbour, Hong Kong. Malacological Review 16: 99–100 Johnson CR, Chapman RDO (2007) Seaweed invasions: introduction and scope. Botanica Marina 50: 321–325 Kalyanasundaram N (1975) Studies on the biology of Mytilopsis sallei (Recluz), an important marine fouling mollusc. Bulletin of the Department of Marine Science, University of Cochin 7: 658–693 Kauano RV, Roper JJ, Rocha RM (2017) Small boats as vectors of marine invasion: experimental test of velocity and desiccation as limits. Marine Biology 164: 27, https://doi.org/10.1007/s00227-016-3057-x Keller RP, Drake JM, Drew MB, Lodge DM (2010) Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network. Diversity and Distribution 17: 93–102, https://doi.org/10.1111/j.1472-4642.2010.00696.x LCP (2018) Laem Chabang Port statistics. https://www.laemchabangportnew.com (accessed 15 November 2018) Lim JY, Tay TS, Lim CS, Lee SSC, Teo SL-M, Tan KS (2018) Mytella strigata (Bivalvia: Mytilidae): an alien mussel recently introduced to Singapore and spreading rapidly. Molluscan Research 38: 170–186, https://doi.org/10.1080/13235818.2018.1423858 McFarland K, Baker SM, Baker P, Rybovich M, Volety AK (2014) Temperature, salinity, and aerial exposure tolerance of the invasive mussel, Perna viridis, in estuarine habitats: implications for spread and competition with native , Crassostrea virginica. Estuaries and Coasts 38: 1–10, https://doi.org/10.1007/s12237-014-9903-5 Mediodia DP, De Leon SMS, Anasco NC, Baylon CC (2017) Shell morphology and anatomy of the Philippine charru mussel Mytella charruana (d’Orbigny, 1842). Asian Fisheries Science 30: 185–194 Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Frontiers in Ecology and the Environment 6: 485– 492, https://doi.org/10.1890/070064 Morton B (1980) Mytilopsis sallei recorded from Hong Kong: an introduction by Vietnamese refugees? Malacological Review 13: 90–92 Morton B (1981) The biology and functional morphology of Mytilopsis sallei (Récluz) (Bivalvia: Dreissenacea) fouling Visakhapatnam Harbour, Andhra Pradesh, India. Journal of Molluscan Studies 47: 25–42, https://doi.org/10.1093/oxfordjournals.mollus.a065555 NIMPCG (2010a) Marine Pests Monitoring Manual: Version 2.0. National Introduced Marine Pests Coordination Group, Department of Agriculture, Fisheries and Forestry, Canberra, 142 pages NIMPCG (2010b) Australian Marine Pests Monitoring Guidelines: Version 2.0. Department of Agriculture, Fisheries and Forestry, Canberra, 55 pages NIMPIS (2017) National Introduced Marine Pests Information System. http://data.daff.gov.au/ marinepests/ (accessed 25 December 2017) Rice MA, Rawson PD, Salinas AD, Rosario WR (2016) Identification and salinity tolerance of the western hemisphere mussel Mytella charruana (d’Orbigny, 1842) in the Philippines. Journal of Shellfish Research 35: 865–873, https://doi.org/10.2983/035.035.0415 Rilov G, Benayahu Y, Gasith A (2004) Prolonged lag in population outbreak of an invasive mussel: a shifting-habitat model. Biological Invasions 6: 347–364, https://doi.org/10.1023/b: binv.0000034614.07427.96 Sanpanich K (2011) Marine bivalves occurring on the east coast of the Gulf of Thailand. ScienceAsia 37(37): 195–204 SCAISTF (2007) South Carolina Aquatic Invasive Species Management Plan. South Carolina Aquatic Invasive Species Task Force, South Carolina Department of Natural Resources, Charleston, SC, USA, 136 pp, https://doi.org/10.3934/molsci.2017.4.446 Seebens H, Gastner MT, Blasius B (2013) The risk of marine bioinvasion caused by global shipping. Ecological Letters 16: 782–790, https://doi.org/10.1111/ele.12111 Stenyakina A, Walters LJ, Hoffman EA, Calestani C (2010) Food availability and sex reversal in Mytella charruana, an introduced bivalve in the southeast United States. Molecular Reproduction and Development 77: 222– 230, https://doi.org/10.1002/mrd.21132 Tan KS, Morton B (2008) The invasive Caribbean bivalve Mytilopsis sallei (Dreissenidae) introduced to Singapore and Johor Bahru, Malaysia. Raffles Bulletin of Zoology 54: 429–434 Thomson JM (1952) The acclimatization and growth of the Pacific oyster (Gryphaea gigas) in Australia. Australian Journal of Marine and Freshwater Research 3: 64–73, https://doi.org/ 10.1071/mf9520064 Thomson JM (1959) The naturalization of the Pacific oyster in Australia. Australian Journal of Marine and Freshwater Research 10: 144–149, https://doi.org/10.1071/mf9590144

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 355 Mytella strigata in Southeast Asia

TWAP (2018) LME 35 – Gulf of Thailand. Transboundary Water Assessment Programme, 13 pp. http://onesharedocean.org/public_store/lmes_factsheets/factsheet_35_Gulf_ofThailand.pdf2015 (accessed 21 November 2018) Vallejo B Jr, Conejar-Espedido J, Manubag L, Artiaga KCC, Damatac II AM, Imperial ICVJ, Itong TAB, Fontanilla IK, Cao EP (2017) First record of the Charru mussel Mytella charruana d’Orbigny, 1846 (Bivalvia: Mytilidae) from Manila Bay, Luzon, Philippines. BioInvasions Records 6: 49–55, https://doi.org/10.3391/bir.2017.6.1.08 Wangkulangkul K (2018) Comments on restricted distribution of Mytilopsis adamsi Morrison, 1946, a non-native false mussel in the Songkhla Lagoon System, southern Thailand. Limnology 19: 151–156, https://doi.org/10.1007/s10201-017-0515-1 Wangkulangkul K, Lheknim V (2008) The occurrence of an invasive alien mussel Mytilopsis adamsi Morrison, 1946 (Bivalvia: Dreissenidae) in estuaries and lagoons of the lower south of the Gulf of Thailand with comments on their establishment. Aquatic Invasions 3: 325– 330, https://doi.org/10.3391/ai.2008.3.3.7 Wells FE, McDonald JI, Huisman JM (2009) Introduced marine species in Western Australia. Western Australian Department of Fisheries, Perth Fisheries Occasional Publications 57: 1–97 Wikipedia (2018) Port of Bangkok. https://en.wikipedia.org/wiki/Port_Authority_of_Thailand (accessed 22 September 2018) Willan RC, Russell BC, Mufet NB, Moore KL, McEnnulty FR, Horner SK, Hewitt CL, Dally GM, Campbell ML, Borke ST (2000) Outbreak of Mytilopsis sallei (Récluz, 1849) (Bivalvia: Dreissenidae) in Australia. Molluscan Research 20: 25–30, https://doi.org/10.1080/13235818. 2000.10673730 Yuan W, Walters LJ, Schneider KR, Hoffman EA (2010) Exploring the survival threshold: a study of salinity tolerance of the nonnative mussel Mytella charruana. Journal of Shellfish Research 29: 415–422, https://doi.org/10.2983/035.029.0218

Supplementary material The following supplementary material is available for this article: Table S1. Locations surveyed for Mytella strigata and Mytilopsis sallei in the inner Gulf of Thailand. This material is available as part of online article from: http://www.reabic.net/journals/bir/2019/Supplements/BIR_2019_Sanpanich_Wells_Table_S1.xlsx

Sanpanich and Wells (2019), BioInvasions Records 8(2): 343–356, https://doi.org/10.3391/bir.2019.8.2.16 356