Aquatic Invasions (2020) Volume 15, Issue 4: 646–670

CORRECTED PROOF

Review Checklists, production trends, and potential ecological and socioeconomic impacts of non-native freshwater in : a review

Abdulwakil Olawale Saba1,2, Ahmad Ismail1, Syaizwan Zahmir Zulkifli1, Shamarina Shohaimi1, Nor Rohaizah Jamil3, Nolila Mohd Nawi4, Intan Faraha A. Ghani5, Muhammad Rasul Abdullah Halim6 and Mohammad Noor Azmai Amal1,* 1Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia 2School of Agriculture, Lagos State University, 106101 Epe Campus, Lagos, Nigeria 3Department of Environmental Sciences, Faculty of Environmental Studies, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia 4Department of Agribusiness and Bioresource Economics, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia 5Department of Science and Biotechnology, Faculty of Engineering and Life Sciences, Universiti Selangor, Bestari Jaya Campus, 45600 Bestari Jaya, Selangor, Malaysia 6School of Biological Sciences, Universiti Sains Malaysia, 11800 Gelugor, Penang, Malaysia Author e-mails: [email protected] (AOS), [email protected] (AI), [email protected] (SZZ), [email protected] (SS), [email protected] (NRJ), [email protected] (NMN), [email protected] (IFAG), [email protected] (MRAH), [email protected] (MNAA) *Corresponding author

Citation: Saba AO, Ismail A, Zulkifli SZ, Shohaimi S, Jamil NR, Nawi NM, Ghani IFA, Halim MRA, Amal MNA (2020) Abstract Checklists, production trends, and potential ecological and socioeconomic impacts of The importation of non-native into Malaysia began as early as the 19th non-native freshwater fishes in Malaysia: century, when a substantial number of non-native fishes were introduced from a review. Aquatic Invasions 15(4): 646– 670, https://doi.org/10.3391/ai.2020.15.4.07 southern China, heralding the beginning of aquaculture in Malaysia. In this review, we analyzed the available literature on the history, checklists, current status, Received: 6 January 2020 production trends, and potential ecological and socioeconomic impacts of non-native Accepted: 10 June 2020 freshwater fishes in Malaysia. We identified a total of 30 non-native food fishes Published: 16 October 2020 belonging to 12 families, with Cichlidae occurring the most frequently. Moreover, Handling editor: Darrah Wooford 173 species from 40 families of non-native freshwater ornamental, recreational and Thematic editor: Ian Duggan biological control fishes were also listed. The aquaculture production and wholesale value were significantly higher (p < 0.05) for non-native species, as compared to Copyright: © Saba et al. This is an open access article distributed under terms native species. Approximately 93% (1,317,990 metric tonnes (MT)) of aquaculture of the Creative Commons Attribution License production and 85.6% (RM 7.4 billion) of wholesale value are from non-native (Attribution 4.0 International - CC BY 4.0). species. However, for inland freshwater captured fisheries, the landing and wholesale OPEN ACCESS. values were significantly higher (p < 0.05) for native species than the non-native species. Non-native species only occupied approximately 28.6% (18,227 MT) of the landing, and 14.2% (RM 110 million) of wholesale value, respectively. For the ornamental fish production, the highest value was recorded in the year 2012 (RM 629 million), but dipped to its lowest value in 2017 (RM 327 million). The cyprinids that are mostly represented by non-native species recorded the highest value (RM 112 million) in the year 2018, followed by osteoglossids that are mainly represented by the native Asian (RM 108 million). Despite the massive economic contribution from these non-native fishes, some of these fish present important ecological and socioeconomic threats to Malaysia. Several recommendations are proposed for a win-win situation between the economic gains and environmental threats caused by these non-native fishes.

Key words: aquaculture, fish, inland fisheries, introduced fish, native biodiversity, invasive fish

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Introduction Biodiversity is an indicator of the health of ecosystems (Shao et al. 2019). High levels of species extinction have been associated with loss of biodiversity (Chong et al. 2010). Although some other challenges to ecosystem health have been identified such as degradation, over-exploitation, pollution, endemism, and anthropogenic factors, the impacts of invasive non-native species should not be neglected (Chong et al. 2010; Tarkan et al. 2015). The negative impacts of non-native fishes have been widely debated (Khairul-Adha 2012). However, non-native fishes are commonly consumed as food, used for recreational activities such as sport fishing and fish keeping, helps to generate income and employment for those involved in the culture, processing, and marketing of these fishes (Ciruna et al. 2004; Britton and Orsi 2012; Yusoff 2015; Bartley and Funge-Smith 2018). Moreover, non-native freshwater fish species, such as tilapia (Oreochromis sp.) and (Clarias sp.) have contributed more than RM 650 million to Malaysia annually (Department of Fisheries (DOF) 2016). In the future, there is a high potential for increasing production of non-native fish species, as a contribution to fish production to meet the needs of the growing population in Malaysia (Yusoff 2015). Indeed, the non-native ornamental fish industry in Malaysia not only generates foreign exchange for the country, but also jobs for a certain proportion of the population (Ng 2016). The initial importations of live fish to Malaysia were for aquaculture, the aquarium trade, recreation, and biological control (Khairul-Adha et al. 2013). However, if the imported non-native fish escaped or were intentionally released into the local waters, it could potentially introduce new diseases, compete for food and space with native species, cause hybridization, and lead to the extinction of endemic and native fish species (Cucherousset and Olden 2011). Details of non-native freshwater fish species in Malaysia are incomplete with regards to past trends and possible recent introductions. Thus, there is a need to collate and analyze their current status and potential environmental and socioeconomic impacts. This paper analyses the available literature on the history, checklists, current status, production trends, and potential ecological and socioeconomic impacts of non-native freshwater fishes in Malaysia.

The methodology of the review Through analysis of research from published journals, recent news reports (within the last decade) and grey literature, information on the history, diversity, ecological impacts, and status of non-native fish species in Malaysia were summarised and synthesized. The Google Scholar database was utilized to find relevant information (history, socioeconomic and ecological impacts) using keywords such as “alien”, “non-native”,

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“invasive” and “non-indigenous”. In order to obtain the most relevant results, these keywords were combined in different ways by varying the use of Boolean operators such as “AND” and “OR”. Publications from the 1980s until the present time were considered for the review to cover historical aspects. Our searches included peer-reviewed publications and policy documents from the Malaysian government and international organizations (e.g. FAO). Recent news articles were also considered in the review. Two separate checklists of non-native freshwater fish species were prepared. The first list consists of fishes that are used mainly for food, whereas the second consists mainly of ornamental, recreational and biological control species, imported to Malaysia since the 19th century. The nomenclature and families to which they belong were validated using Rainboth (1996), Kottelat (2013), FishBase (Froese and Pauly 2019), Zakaria- Ismail et al. (2019), and Catalogue of Fishes (Fricke et al. 2020). To avoid duplications and discrepancies, all species that appeared more than once and those with unverifiable nomenclature were excluded from the lists. Secondary data on freshwater fish aquaculture and those of inland capture fisheries between 2007 and 2018 were accessed online from the Department of Fisheries (DOF), Ministry of Agriculture and Food Industries, Malaysia (www.dof.gov.my). Data unavailable online were obtained by visiting the DOF Data Unit in Putrajaya, Malaysia. All these data were used to generate trend analyses of native versus non-native freshwater fish production and wholesale values, as well as analysis by species produced from freshwater aquaculture and inland capture fisheries. The data on ornamental fish species from 2010 to 2017 were also collected from the DOF website (www.dof.gov.my) and used for trend analysis of production and value. To determine if differences exist between non-native and native fish production by weight and wholesale value for freshwater fish culture and inland capture fisheries, a Mann-Whitney U test was performed using IBM SPSS Statistics 2015 for Windows, Version 23.0., Armonk, NY, USA. Descriptive analyses and graphs were prepared using Microsoft Excel 2016 (Microsoft Inc., USA), and to conveniently identify the non-native fish production hotspots to inform possible management measures, the relative production levels of non-native freshwater aquaculture, inland capture fisheries, and ornamental fish was presented geospatially through the use of ArcGIS desktop (ESRI, USA). Georeferenced data sets for all states in Malaysia were imported as shapefiles to ArcGIS version 10.2, after which non-native freshwater aquaculture, inland capture fisheries and ornamental fish production according to the state were combined with the georeferenced data.

The history of fish introduction to Malaysia A substantial number of fish species were imported to Malaysia as early as the 19th century by the southern Chinese (Mohsin and Ambak 1983; Ang et

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al. 1989; Ali 1998; DOF 2007b). This heralded the beginning of aquaculture in Malaysia through the widespread polyculture of Chinese carps such as bighead carp (Hypophthalmichthys nobilis), silver carp (H. molitrix) and grass carp (Ctenopharyngodon idella) (Welcomme 1989; Mazuki 2008). Fish importation continued after the Second World War when some non- native fish species were brought in for aquaculture, recreation and the aquarium fish industry by governmental and semi-governmental bodies, including the private sector and private individuals (Welcomme 1989; DOF 2007b). Introduction for culture purposes was identified as the primary mode of spread with other routes, such as stocking to improve fisheries, aquarium business, sport fishing and biological control (DOF 2007b; Chong et al. 2010). The spread of these species into Malaysian aquatic ecosystems was enhanced by unintentional translocation, which includes the use of non-native fishes as fish bait, release and/or escape from fish farms and the dumping of undesirable aquarium fishes for specific reasons that include unmanageable size and, in some cases, religious purposes (Khairul-Adha et al. 2013).

Non-native fish species checklists in Malaysia The comprehensive review from available literature showed that a total of 30 non-native food fishes, belonging to 12 families, have been reported in Malaysia (Supplementary material Table S1). Cichlidae and Cyprinidae occurred the most with seven and six species, respectively, followed by Xenocyprididae with five species. Furthermore, a total of 173 species from 40 families of non-native freshwater ornamental fishes were identified. Family Cichlidae had the highest number of species (67 species), followed by Characidae (27 species) and Cyprinidae (11 species) (Table S2). All other families had between one to seven species, and many of the species were reported to have had more than one variety, in some cases, up to 30 (DOF 2007b). The list is made up of not only ornamental fishes, but also recreational and biological-control fishes. Most of the ornamental fishes are reportedly bred in Malaysia, with only some of them known to be established in public waters (DOF 2007b; NCIAS 2018).

Non-native food fish culture in Malaysia Tilapia, African , striped catfish, and carps are among the most harvested freshwater fishes in Malaysia (DOF 2018). However, all of these species did not originate from Malaysia (Welcomme 1989; Rainboth 1996; Froese and Pauly 2019).

Tilapia Tilapia were imported to Malaysia to increase access to a cheap source of protein. Mozambique tilapia (Oreochromis mossambicus) was brought from

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Indonesia in 1944, and its breeding was undertaken by government hatcheries (Ang et al. 1989). It turned out to be the most popular tilapia species cultured in Malaysia (Liong et al. 1988; Mazuki 2008). Furthermore, Nile tilapia (O. niloticus) and the red hybrid tilapia (O. niloticus × O. mossambicus) were imported from in 1979 (Ang et al. 1989; Mazuki 2008). Commercial production of all-male tilapia through the “Genetically Improved Fish Tilapia (GIFT)” program was the genesis of monosex tilapia culture, which led to even higher productivity (Mazuki 2008). Over 30 years ago, the cage culture of Nile tilapia had been undertaken in Lake Kenyir, Terengganu, by DOF Malaysia and the private sectors (DOF 2007b). At that time, there was a strong recommendation for its further culture due to its economic viability and social acceptance. In addition to this, there were significant efforts to prevent its escape into local waters to avoid establishment in the wild (DOF 2007b). As of 1992, different strains of tilapia were responsible for about one-fifth of the total production from freshwater ponds, while others, particularly the red hybrid tilapia, were grown in concrete tanks under very intensive systems (Kechik 1995). Recently, the culture of tilapia has been practised throughout Malaysia in various types of water bodies, including reservoirs, ex-mining pools, irrigation canals and rivers (Zamri-Saad et al. 2014).

Catfishes Catfishes, including African catfish (Clarias gariepinus), channel catfish (Ictalurus punctatus), striped catfish (Pangasianodon hypophthalmus) and the hybrid catfish (C. macrocephalus × C. gariepinus) are also cultured in Malaysia (DOF 2007b, 2018). These species became popular with fish farmers because of their hardiness, high fecundity, fast growth rate and ease of culture (Kechik 1995). The non-native catfishes of Malaysia belong to five different families, including Clariidae (air-breathing catfishes), Pangasiidae (shark catfishes), Ictaluridae (bullhead catfishes), (long-whiskered catfishes) and Bagridae (bagrid catfishes) (DOF 2007b). According to DOF (2007b), the African catfish was imported to Malaysia in 1988. However, Dauda et al. (2018) traced its importation to sometime between 1986 to 1989, with the first report of their culture in 1987, while the channel catfish was reportedly introduced from Cuba in 2001 for culture purposes (DOF 2007b). Previously, Khairul-Adha et al. (2013) categorized bighead catfish (C. macrocephalus) as non-native fish in Malaysia. However, we believe bighead catfish is a native species of . Even though the bighead catfish was reportedly introduced from Thailand in 1950 for aquaculture purposes (Welcomme 1989), the status of bighead catfish in Peninsular Malaysia is uncertain. The records of this species in Peninsular Malaysia was only known in the early 1950s with specimens reported from Terengganu and (Tweedie 1952). It might very well be

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native to Peninsular Malaysia and unnoticed by fisheries biologists. Thus, we treat bighead catfish as native fish species in this review. Catfish species from the family Pangasiidae, including yellowtail catfish (Pangasius pangasius), striped catfish (Pangasianodon hypophthalmus) and giant catfish (Pangasius sanitwongsei) were imported for aquaculture purposes (Welcomme 1989; DOF 2007b). The origin of the giant catfish could not be ascertained, but the other two species were attributed to Thailand and , respectively (DOF 2007b). The establishment status of African catfish (C. gariepinus) is yet to be confirmed; however, it has been reported alongside the non-native midas cichlid (Amphilophus citrinellus) and gobiid fish (Rhinogobius similis) collected from the rice agroecosystem in Seberang Perai Tengah, Penang (Aqmal-Naser and Ahmad 2018). Asian redtail catfish (), which is the only non-native species from the family Bagridae, was probably imported for aquaculture purposes (NCIAS 2018). Finally, redtail catfish (Phractocephalus hemioliopterus), belonging to the family Pimelodidae, was imported as an aquarium fish (DOF 2007b).

Carps Chinese carps, including grass carp (Ctenopharyngodon idella), bighead carp (Hypophthalmichthys nobilis), silver carp (H. molitrix) and common carp (Cyprinus carpio), were imported through the immigration of southern Chinese in the 1800s, coupled with the introduction of polyculture practices (Welcomme 1989; DOF 2007b). In 1969, bighead carp was successfully spawned artificially in the tropical fish culture research institute in Malacca, Malaysia (DOF 2007b). Apart from the supply of common carp, bighead carp and grass carp, which comes mainly from the government-owned hatcheries, common carp were also sourced from a few private hatcheries (Liong et al. 1988). Also, approximately 3,000 fingerlings of Indian carps, such as catla (Labeo catla), rohu (L. rohita) and mrigal (Cirrhinus cirrhosus) were brought into Malaysia from India between 1957 and 1970 (Khan and Jhingran 1975; Welcomme 1989; DOF 2007b). Some other carps, such as Javanese barb (Barbonymus gonionotus) and grass carp (C. idella), were also obtained from government-owned hatcheries and later cultured in cages (Liong et al. 1988; Kechik 1995). One of the very important freshwater fish species cultured in Malaysia is the Javanese barb, initially known as Puntius javanicus, brought into Malaysia through in 1953 (DOF 2007b). However, its first introduction was traced back to 1958 (Ang et al. 1989). It was subsequently bred by the DOF Malaysia for onward distribution to fish aquaculturists. Furthermore, the Malaysian government facilitated the release of approximately 120,000 individuals of Javanese barb into inland water bodies throughout the country, and in a

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bid to further enlarge the gene pool, this species was re-introduced from Thailand and Indonesia in the 1970s and 1980s (Liong et al. 1988; DOF 2007b).

Non-native ornamental and recreational fishes in Malaysia As early as the 1950s, the aquarium fish industry had been established and attracted much attention with high demands for fish and supplies (Ng 2016). The industry was promoted by the growth of the trade-in ornamental fishes leading to extensive importation of freshwater and marine species from all parts of the world (Ang et al. 1989). As of the 1980s, breeding and culture of these aquarium fishes became prominent, and farms were situated mainly in the southern part of Peninsular Malaysia (Kechik 1995). This influenced, to a large extent, the number of intentional and unintentional introductions of non-native ornamental fishes into the inland water bodies (DOF 2007b). Malaysia has been identified as one of the main producers of ornamental fishes in the world. However, most of the fish species represented in the aquarium industry are non-native (Kechik 1995; DOF 2007b). As reported by DOF (2007b), in total, about 186 species (74%) of the ornamental fishes in Malaysia are non-native. As of 2002, Malaysia produced almost 408 million tails of ornamental fishes, and approximately 259 ornamental fish exporters are present in Malaysia (Ng 2016). Approximately 387 million (95%) fish were exported mainly to the European Union (DOF 2007b). This sizeable industry has not only created jobs, but also contributed to the national income through exportation (Yusoff 2015). However, ecological sustainability remains a concern since the aquarium trade has been noted to be a source of alien fishes introduction (Maceda-Veiga et al. 2013). Before the 1950s, a few species were reared in the backyards of individuals, who mostly sourced their seeds from rivers. As time went on, natural stocks began to deplete; as such, increased farming of ornamental fish species became necessary (Ng 2016). Since this time, there has been rapid growth and spread of the ornamental fish industry across Malaysia. By 1995, over 250 million ornamental fishes valued at USD 19.6 million were produced, and in 2006, this figure had increased to 306 million tails with a value of USD 18.9 million (DOF 2007b). More recently, in 2014, the production reached approximately 393 million individuals valued at approximately US 85 million (DOF 2014). Recreational or sport fishing has only recently gained acceptance in Malaysia, and non-native fish species were introduced for this purpose (Yusoff et al. 2006). This sector is growing rapidly at approximately 15% annually, as a result of increased affluence of the population and leading to increasing demand by the well-to-do in society. Therefore, this sector has a high potential to generate significant revenue, contributing to the country’s

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foreign exchange and economic growth (Yusoff et al. 2006). Despite the increased importation of non-native aquarium fish into the country, there is a lack of documentation and adequate record-keeping regarding the importation of non-native ornamental fishes in Malaysia (Khairul-Adha et al. 2013). The butterfly peacock bass (Cichla ocellaris), locally known as “ikan raja”, is a native of , and has been reportedly introduced deliberately by anglers into several small ponds and mining pools in various places in Malaysia (NWGIAS 2014; Razak 2017; Zulkefli 2017; Zakaria and Bahrin 2018). The peacock bass is a ravenous predator and feeds on a wide variety of prey; therefore, it has the potential to modify the habitat to which it is introduced (Gomiero and Braga 2004; Novaes et al. 2004). The availability of varying size classes of this fish in some ex- mining pools suggests a high probability of its establishment in Malaysia's local waters (Khairul-Adha 2006, 2012). Furthermore, ornamental suckermouth catfish (), Amazon sailfin catfish (Pterygoplichthys pardalis) and vermiculated sailfin catfish (P. disjunctivus) were also reported in Mengkibol River, Johor (Chow et al. 2016), Langat River, Selangor (Samat et al. 2008, 2016) and Pusu River, Selangor (Jalal et al. 2018), respectively. According to Khairul- Adha et al. (2013), researchers have recorded non-native species like tilapia (O. niloticus) and vermiculated sailfin catfish (P. disjunctivus) from local waters within the past few decades.

Non-native fish production Aquaculture The freshwater non-native culture fish production from 2007 to 2018 was significantly (U = 0.000, p < 0.001) higher for non-native species (Mdn = 103,503.46 metric tonnes (MT)), than native species (Mdn = 7,172.31 MT). Similarly, the wholesale value was significantly (U = 0.000, p < 0.001) higher for non-native species (Mdn = RM 633,057.31) than for native species (Mdn = RM 87,500.82). Non-native species dominate the freshwater aquaculture production. Out of the 1,418,709 MT of fish produced with a wholesale value of RM 8.6 billion from 2007 to 2018, approximately 93% (1,317,990 MT) with a wholesale value of approximately RM 7.4 billion (85.6%) are from species not native to Malaysia (Figure 1). The observed significant differences and trends display the critical role played by non-native fishes in Malaysian aquaculture. For the most part, this situation may have been due to deliberate introduction and intervention by the government through the DOF Malaysia in the development of non- native fish aquaculture, due to the need to increase production using candidates of good culture characteristics (Yusoff 2015). Paradoxically, some of these introduced species have not only established breeding populations, but also have the potential to generate some negative environmental impacts

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Figure 1. The trend in non-native versus native freshwater aquaculture fish production by weight and wholesale value from 2007–2018. Adapted from DOF (2007–2018).

such as competition with native species for food and space, predation on juveniles and eggs of native species, and disruption of the habitat by grazing on detritus and benthic algae (Canonico et al. 2005; Abraham 2011; Ansah et al. 2014). As a result, the non-native fishes may cause habitat alteration or reduction in food availability and the physical cover available for aquatic consumed by other native fishes (Mendoza et al. 2009; Hussan et al. 2016). The trend in non-native fish production and wholesale value by species is shown in Figure 2. The figures indicate that freshwater catfish (Clarias) had the highest total production of 555,822 MT between 2007 and 2018. This is followed by the red tilapia (Oreochromis hybrid) and river catfish (Pangasianodon) with a total production of 351,545 and 194,239 MT, respectively. Indian carps, snakeskin gourami (Trichopodus pectoralis), and jade perch (Scortum barcoo) had the lowest production at 10, 82 and 305 MT respectively, within the same period. In 2011, there was a decline in the total non-native freshwater culture fish production, which picked-up in 2012. The data also showed that Perak had the highest production of non- native freshwater aquaculture fish, followed by Selangor (Figure 3). The two lowest production levels were found in Wilayah Persekutuan Labuan and Perlis. In Perak, river catfish were the most important with the highest production level. However, it may not be the most important by wholesale or retail value. Native fish species with the highest aquaculture production for 2018 included Sultan fish (Leptobarbus sp.) (1,771 MT), river catfish (Hemibagrus sp.) (1,527 MT), snakehead (Channa striata) (510 MT) and climbing perch (Anabas testudineus) (662 MT) (DOF 2018). In general, the highest proportion of freshwater fish culture production (93%) was attributed to non-native fish species. Moreover, aquaculture fish

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Figure 2. The trend of non-native freshwater aquaculture fish production by species (A), and wholesale value by species (B) from 2007–2018. Adapted from DOF (2007–2018).

production may continue to increase its contribution in the years to come. This evident success has also been attributed to the great support from the government (Yusoff 2015).

Inland freshwater capture fisheries Figure 4 shows the trend in the landing and value of Malaysia’s non-native and native freshwater capture fisheries, respectively. Native fish landings dominate this sector, out of the total of 63,641 MT of fish landings with a wholesale value of about RM 775 million between 2007 and 2018, non-native species occupied approximately 28.6% (18,227 MT), with a wholesale value of approximately 14.2% (RM 110 million). The freshwater capture fisheries landing was significantly (U = 144.0, p < 0.001) higher for native fish species (Mdn = 3,686.0 MT) than for non-native species (Mdn = 1,360.5 MT).

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Figure 3. (A) Non-native freshwater aquaculture production level by species and state in 2018, and (B) geospatial representation of freshwater aquaculture fish production by state in 2018. Adapted from DOF (2018).

Figure 4. The trend in freshwater non-native versus native capture fisheries landings by weight and wholesale value from 2007–2018. Adapted from DOF (2007–2018).

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Figure 5. The trend in non-native capture fisheries landings by species (A), and wholesale value by species (B) from 2007–2018. Adapted from DOF (2007–2018).

Similarly, the wholesale value was significantly (U = 144.0, p < 0.001) lower for non-native species (Mdn = RM 9,081.50) than for native species (Mdn = RM 48,364.50). The trend in non-native freshwater capture fisheries landings and wholesale value by species indicate that between 2007 and 2018, red tilapia was the most important with the highest landing in weight (8,704 MT) and by value (RM 27 million) (Figure 5). From 2009–2011, there was a general increase in total inland non-native fish landing after there was a fall that picked-up again from 2014–2016. Similar to the non-native culture fish production, many factors including climate change, changes in fishing effort, and market demand could be responsible for this fluctuation (Barange and Perry 2009). Furthermore, the value of these species seems to be increasing despite the seemingly steady production values from 2016– 2018. As with aquaculture production, Perak maintained its lead with the

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Figure 6. (A) Non-native freshwater capture fisheries landing level by species and state in 2018, and (B) geospatial representation of inland freshwater non-native capture fisheries landing by state in 2018. Adapted from DOF (2018).

highest non-native fish landings with 421 MT, closely followed by Sarawak with 281 MT, but Melaka with no production (Figure 6). In Perak, the fish with the highest production by weight was red tilapia at 197 MT, whereas rohu recorded the lowest at 2.2 MT. As of 2018, species such as river catfish (Hemibagrus sp.) (524 MT), tinfoil barb (Barbonymus schwanefeldii) (473 MT), snakehead (C. striata) (167 MT), marbled goby (Oxyeleotris marmorata) (140 MT), climbing perch (A. testudineus) (133 MT), hard-lipped barb (Osteochilus wandersii) (115 MT), hampala barb (Hampala macrolepidota) (108 MT) and crossbanded barb (Puntioplites bulu) (104 MT) were among the highest landing native fish species from inland capture fisheries in Malaysia (DOF 2018).

Ornamental fish From 2010 to 2017, the ornamental fish production (in terms of the number of individuals) showed that the highest production in 2016, whereas the lowest was in 2011 (Figure 7). Poecilids had the highest total production in number, with loricariids being the lowest. The highest value of ornamental fish production was recorded in the year 2012 at approximately RM 629 million. This value dipped to its lowest value in 2017 at approximately

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Figure 7. The trend in the production (A) and value (B) of ornamental fishes by family from 2010–2018. Adapted from DOF (2010–2018).

RM 327 million. While there was an increase in the production of all other fish families, cyprinids which are mostly represented by non-native species recorded the highest production with an approximate value of RM 112 million, followed by osteoglossids which are mostly represented by the native Asian arowana ( formosus) that showed the second- highest total value of approximately RM 108 million. In the case of ornamental fish production by the number of individuals for 2018, Johor was the leading state, producing 2.6 billion individuals valued at approximately RM 231 million (Figure 8). This was followed by Perak, and the lowest production was recorded for Perlis, with Negeri Sembilan having no recorded production. In Johor, cyprinids were recorded to have the highest production by the number of individuals, followed by poecilids, whereas osteoglossids were recorded to have the lowest.

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Figure 8. (A) Ornamental fish production by species and state in 2018, and (B) geospatial representation of ornamental fish production by states in 2018. Adapted from DOF (2018).

Ecological impacts and threats of non-native fishes in Malaysia Non-native fish species may exert negative ecological impacts and threats on native aquatic systems. Among other factors that aid the non-native fish in their successful invasion of new aquatic including their ability to withstand suboptimal water quality levels, prolific spawning capacity, and the ability to live off a wide variety of food (Hussan et al. 2016). For example, sailfin catfish (Pterygoplichthys spp.) were believed to displace several species of native minnows in Texas, USA, including some of the threatened and vulnerable species (Mendoza et al. 2009). The establishment success of different species of tilapiine cichlids was reported to range between 60% and 90% when they get introduced into new open waters (Pullin et al. 1997). In the new habitat, they predated on eggs and small fish in a subtropical Australian impoundment (Arthington et al. 1994). Moreover, Nile tilapia (O. niloticus) replaced native species in Thailand and were reported to be a pest in open waters after excessive reproduction success (De-Iongh and Van-Zon 1993). The conservation of a near threatened clariid catfish (Clarias dussumieri) which is endemic to the West of India was much challenged because it competed with African catfish (Abraham 2011). Judging from the existing impacts of these non-native fish species,

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some of which have established breeding populations in Malaysia’s inland waters, there is a high potential of similar or more significant impacts. Some non-native fish species tend to limit the survival of indigenous taxa, thus threatening biodiversity (Khairul-Adha et al. 2013; MNRE 2014). Such impacts which include predation, competition, and habitat degradation have been experienced in other countries such as the USA (Mendoza et al. 2009), Thailand (De-Iongh and Van-Zon 1993), Iran (Esmaeili et al. 2014) and India (Abraham 2011). In Malaysia, non-native fish species currently occupy diverse ecosystems that include, but not limited to lakes, reservoirs, rivers, swamps, streams, drainage areas, and mining pools (Khairul-Adha et al. 2013; Ng et al. 2017; Zakaria 2019). Non-native species such as piranha (Serrasalmus sp.), pirarucu (Arapaima sp.), African catfish (C. gariepinus), peacock bass (C. ocellaris), striped catfish (P. hypophthalmus) and tilapia (Oreochromis sp.) are readily found in Malaysia’s inland water ecosystems, mostly because of purposeful introduction into local waters (Zakaria 2017). Most of these species grow rapidly, are well adapted to the environment, and feed on local fishes, while some are considered highly invasive (Chong et al. 2010; NWGIAS 2014). For example, non-native species such as tilapia and carp were found in highland streams at Kelalan River, Sarawak (Khairul-Adha et al. 2013), and tilapia were found in Beris and Muda lakes, Kedah (Sharifudin and Sharip 2020). Moreover, Chong et al. (2010) reported that tilapia was considered to be invasive due to their rapidly growing numbers and ability to displace native species in lakes and ponds. However, to the best of our knowledge, there is currently no published study concerning the specific ecological and socioeconomic impacts of these species in Malaysia. The predatory peacock bass (Cichla sp.) was deliberately introduced into Peninsular Malaysia and was released into a lake made from a former mining area by anglers in the early 1990s for sport fisheries (Khairul-Adha 2006). Apart from being piscivorous, the peacock bass grows to very large sizes. The peacock bass has been reported to cause damage to ecosystems because of its highly predatory behaviour, feeding extensively on smaller native fish sizes (NCIAS 2018). Furthermore, peacock bass was said to heavily prey on approximately 50,000 fry of tinfoil barb (B. schwanefeldii) that were released into Timah Tasoh Lake, Perlis by the DOF Malaysia, to boost the native fish population of the lake (Isa et al. 2012; Zulkefli 2017). The mosquitofish (Gambusia affinis), which was recently recorded in Lake Kenyir, Terengganu, is an invasive fish species that can negatively impact freshwater biodiversity and thus hamper the lake’s ability to offer necessary ecosystem services (Walton et al. 2016). Apart from the negative impacts, this species may benefit other larger predators existing in the lake (Walton et al. 2016). Furthermore, it is noteworthy that this species, because of the scale and severity of its impacts in aquatic ecosystems around the world, made a list of 100 of the worlds’ worst invasive species (Lowe et al.

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2000). Although the mosquitofish was reportedly introduced for biological control (Khairul-Adha et al. 2013), there remains a scarcity of accurate information on its introduction date, location, and ecological impacts. Aquarium species such as algae suckermouth catfish (Hypostomus sp.), flowerhorn (Cichlasoma hybrid), (C. carpio), Amazon sailfin catfish (P. pardalis), pirarucu (Arapaima gigas) and (Atractosteus spatula) that were cherished by aquarists are known to have established and exerted negative ecological impacts in some parts of the world (Sumanasinghe and Amarasinghe 2013; Hilgers et al. 2018). Some of these non-native fishes are very interesting to keep during their fingerling and juvenile stages. However, they grow to be large and become less attractive and too costly to manage. Therefore, hobbyists are likely to dispose them into freshwater bodies. Specifically, the flowerhorn, a very prolific producer possessing a voracious appetite can survive harsh conditions, making it a potential ecological threat (DOF 2007b; Hilgers et al. 2018). To date, the actual impacts of these non-native species on the native environment and species are unknown. The Amazon sailfin catfish (P. pardalis) has established a self-breeding population in Langat River, Selangor, with peak spawning during high water levels between September and January (Samat et al. 2016). Moreover, according to Tan (2019), more than 10 tonnes of the Amazon sailfin catfish have been caught from the Skudai River, Johor, adding that they have likely outcompeted the native fish species because of their hardy characteristics. They also disrupted the environment since they dig the river bottom to make burrows to lay eggs. As a result, they tend to contribute to erosion and sedimentation of the river bottom (Hussan et al. 2016). The earth eater (Geophagus steindachneri) and the black ghost knifefish (Apteronotus albifrons) have reportedly been encountered in fish catches in Malaysia (Zakaria 2017). For example, the earth eater was caught in freshwater bodies in Perlis, Selangor, and Johor, whereas the carnivorous black ghost knifefish has been encountered in rivers of Kedah, Perak, and Selangor. The latter generates electrical impulses which, although, weak, may be harmful to other aquatic organisms (Khairuddin and Lionheart 2014; Zakaria 2017). Asian redtail catfish (H. wyckioides) had been reported in catches of fishermen along River, Pahang, whereas the alligator gar (A. spatula) was reported in Selangor River, Selangor (Zakaria 2019). Along with other non-native fish species, these fishes have been implicated in the predation of local fish species in the rivers (Zakaria 2019). They reportedly escaped into the wild from fish farms during severe floods, where they are reared for economic gains. A fish farm operated by Cambodians near Pekan, along the Pahang River, Pahang, may have supplied some of the redtail catfishes (P. hemioliopterus) present in the river (Zakaria 2019).

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Another popular aquarium species is the common carp or koi (C. carpio). This species has contributed to the increase in fisheries revenue. It has, however, contributed to the introduction of diseases to the aquarium industry, such as the Koi Herpes Virus (Azila et al. 2012). Because of the contagious nature of these diseases, they may cause significant mortality or morbidity, with the possibility of causing between 80% to 100% mortality in affected populations. Positive cases of this disease have been detected in the Ulu Kinta, Tronoh, and Gopeng of Perak (DOF 2007b; Azila et al. 2012). Currently, the peacock bass (Cichla sp.), American paddlefish (Polyodon spathula), Asian redtail catfish (H. wyckioides), freshwater stingray (Potamotrygon motoro), flowerhorn (Cichlosoma hybrid), red-striped earth eater (Geophagus surinamensis) and algae sucker catfish (Hypostomus sp.) have been listed as major threats to Malaysia’s native freshwater ecosystems (NCIAS 2018). However, the magnitude of their potential and existing threats is not well-known and may not be quantified due to a lack of scientific evidence. Apart from non-native species introduction, other anthropogenic factors may threaten native fish species diversity (Gozlan et al. 2010). These threats include flow modification, habitat degradation (Johnson et al. 2008), overexploitation, pollution (Dudgeon et al. 2006), and climate change (Kiruba-Sankar et al. 2018). Non-native fishes may also take advantage of these factors to worsen the impacts on the native flora and fauna (Geraldi et al. 2019). However, scientific studies to ascertain the extent of these impacts in Malaysia are scarce.

Socioeconomic impacts of non-native freshwater fishes in Malaysia Most of the analyses in the preceding figures are useful for expressing the magnitude of the non-native fish contribution to Malaysia’s economy, not only in aquaculture but also for inland capture fisheries. Although native ornamental fish such as the Asian arowana (S. formosus) are among the dominating species in the ornamental fish trade, considering its vast contribution by value, it is remarkable that 100% of all species belonging to the family Poeciliidae, which turned out to give the highest production by number and the third-highest by value, are non-native (DOF 2007–2018). The current and potential socioeconomic impacts of non-native fishes can be categorized into positive, negative, and neutral (Kiruba-Sankar et al. 2018). Despite their contribution to economic development, some non- native fishes threaten the biodiversity of native waterbodies. As a result of this, there is a possibility that catches of native fishes will be reduced, thus hampering the earning abilities of the local fishers (Zulkefli 2017). Moreover, some of the non-native species, despite being non-target organisms, also have morphological characteristics capable of destroying the fishing gears, thus putting an additional financial burden on the fishermen due to the need to replace or repair their damaged fishing gears (Khairul-Adha et al.

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2013). In addition to the direct economic impacts of non-native fish species where fishermen suffer losses due to declined catches or damage to their fishing gears, part of the socioeconomic impacts of invasive species may include the cost of their management (Hanley and Roberts 2019). We could not find any current published information on the socioeconomic costs of non-native fish management in Malaysia, and this information is also generally scarce for many countries (Hanley and Roberts 2019). Fish species posing the most significant threats of invasiveness, and waterbodies with important biodiversity should be prioritized for management. This should come after a cost-benefit analysis has been done to achieve optimal results with the least costs. Sportfishing is becoming increasingly popular (Khairul-Adha 2012), and this has been a source of extra income to boat owners who rent them out to sport fishers (Zulkefli 2017). In Malaysia, we observed that members of a particular non-native fish family, especially Loricariidae that have established breeding populations in local waters, are not useful as aquarium fishes as they grow into large sizes and also not preferred as food, probably due to the nature of their skin and flesh. Therefore, these fishes may be used for alternative beneficial purposes such as inclusion in feed as protein sources and other possible industrial applications (Panase et al. 2018; Elfidasari et al. 2019; Anguebes-Franseschi et al. 2019; Herath et al. 2020). The beneficial contribution of non-native fish species through aquaculture and the ornamental fish business to the socioeconomic well-being of many countries and the people including Malaysia, as well as its GDP and foreign exchange is significant (Yakupitiyage and Bhujel 2005; Shelton and Rothbard 2006; Mazuki 2008; Lin et al. 2013). Many jobs have been created through aquaculture, and non-native fish species occupy a considerable proportion of farmed fish production (DOF 2007b; Mazuki 2008). In the freshwater inland capture fisheries sector, the landing of non- native fishes is also increasing. The current production figure, although not as much as 30% of the total 12-year production, may continue to compete with the native fish production.

Conclusion and recommendations Various non-native fish species are important for the Malaysian economy. However, non-native fishes may also have negative consequences on the biodiversity and ecosystems of this country if not properly managed. Thus, the decision framework to produce a win-win situation should be explored to help harness the socioeconomic gains and tackle threats to native biodiversity as detailed in the Food and Agricultural Organization’s Precautionary Approach to Capture Fisheries and Species Introduction. Furthermore, the guidelines require the application of prudent foresight which takes into account uncertainties in fisheries systems and the necessity of acting even with incomplete knowledge (FAO 1996).

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Considering all the information gathered in this study, the following recommendations are proposed:  The Malaysian government, through the DOF under the Ministry of Agriculture and Food Industries, together with the Ministry of Energy and Natural Resources, should continue to implement the strategies detailed in its action plan for non-native aquatic species in Malaysia (DOF 2007b), National Policy on Biological Diversity 2016–2025 (MNRE 2014), and the precautionary approach, including regular monitoring and strict regulations.  Research on public knowledge and stakeholders’ perceptions of the ecological and socioeconomic benefits of non-native fish species is advocated. Thereafter, depending on the outcomes, suitable programs should be designed to educate the public, aquaculturists, and workers in fisheries related-industries on the possible negative impacts of non- native fishes when not managed properly, since they may lack the knowledge regarding possible negative consequences of their actions.  Research and monitoring of the impacts of the non-native species on biodiversity, ecosystems, and socio-economy are urgently needed. This should include invasiveness risk analysis, which is currently lacking.  An economic and biological analysis is needed for widely accepted and farmable native fishes for potential upgrading for intensive culture, ornamental, and scientific purposes.  Possible alternative and more beneficial uses of the less valuable non- native fish species should be considered as a means to generate more benefits (e.g. Amazon sailfin catfish, suckermouth catfish and peacock bass are used for fish or animal feed, in order to serve as a source of protein, and their flesh and skin could be used as a good source of collagen for potential industrial or cosmetic applications).  The general public, as well as anglers, should be encouraged to report cases and assist in conserving native biodiversity through ecosystem friendly practices which may include ensuring that the non-native species do not get released into the local waters and protecting the local waters through community alertness. This can also be facilitated through recognition and possibly, rewarding those who contribute to this cause.

Acknowledgements

The authors appreciate the Department of Fisheries, Ministry of Agriculture and Food Industries, Malaysia, for providing the data on fish production. We also thank the anonymous reviewers for carefully reading the manuscript and providing valuable comments and suggestions.

Funding Declaration

This study was financially supported by the Ministry of Higher Education, Malaysia under the Fundamental Research Grant Scheme (FRGS/1/2018/STG03/UPM/02/11).

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Supplementary material The following supplementary material is available for this article: Table S1. Checklist of non-native food fishes in Malaysia. Table S2. Checklist of alien aquarium, recreational and biological control fishes. This material is available as part of online article from: http://www.reabic.net/aquaticinvasions/2020/Supplements/AI_2020_Saba_etal_SupplementaryTables.xlsx

Saba et al. (2020), Aquatic Invasions 15(4): 646–670, https://doi.org/10.3391/ai.2020.15.4.07 670