Mitigating the role of aquaculture in crustacean invasions

Aquaculture plays a critical role in alleviating malnutrition and poverty1 and stands as the world's fastest growing food sector,2 especially in developing countries.3 Global aquaculture production increased by over 600% from 1990 to 2020,4 accompanied by a diversification of farmed species, reaching 425 species in 2021.5 Notably, the number of crustacean species reared commercially has risen from 30 to at least 49 between 2017 and 2020.4, 6 Many farmed species are non-native in their farmed regions, a trend first observed in 2000 in developing countries such as Cuba, India, Philippines, Chile and Brazil, where 60%–95% of all production is non-native species.7 The growing number of farms and/or farm sizes, along with non-native species farming, increases the risk of intentional or accidental release into the wild.3 This is likely to increase propagule pressure8 as was seen with the redclaw crayfish (Cherax quadricarinatus) which escaped from captivity or abandoned farms and established wild populations in many regions.9 Farmed species are selected for traits which exacerbate their establishment and spread in the wild10 such as rapid growth, broad diet and resistance to parasite.11 Biological invasions, involving human-related introduction, establishment, expansion and potential impact of species outside of their native ecosystem, pose a significant threat to biodiversity and ecosystem functions.12 For example, the red swamp crayfish (Procambarus clarkii) introduced for aquaculture, is now a global invasive species13 which transmits diseases14 and predates on and competes with native species, thereby altering food webs and habitat structures.15 Notwithstanding biological invasions occasional benefits, they do not outweigh their massive economic impacts,16 estimated to be at least USD 423 billions in damage and management,12 also affecting aquaculture itself.17 The signal crayfish (Pacifastacus leniusculus) and the European green crab (Carcinus maenas), collectively inflict damages totalling US $271 million.17 We suggest that the rapid development of farms and farmed species is likely to increase the risk of biological invasion18 unless new biosecurity protocols are developed in parallel.19 While the causal links between aquaculture and biological invasions have been extensively studied for specific countries or species,20-23 substantial gaps remain not least in the case of crustaceans, which are significant both as major aquaculture species and as invaders. Therefore, we focus on farmed crustaceans, although our conclusions apply to other taxonomic groups involved in aquaculture. We show why some farmed crustaceans pose an increasing risk of biological invasions and how this risk can be mitigated. Here, we assess commercially farmed crustaceans classifying them by country (native-non-native) and invasive history (lack or presence of invasions historically). Using these classifications, we recommend biosecurity and management strategies while highlighting the gaps in our current understanding. To compile a comprehensive list of farmed crustacean species, we used the most up to date aquaculture dataset of the Food and Agriculture Organization of the United Nations24 (FAO) and supplemented it with our own literature research. For identifying the invasive crustacean species, we cross referenced multiple invasive alien species databases25-28 ensuring we removed duplicates and validated scientific names using GBIF. Our final dataset includes 63 crustacean species (Appendix S1 & S2) which have been farmed in 126 different countries globally (Table 1; Appendix S3). Here, non-native species are defined as a species outside its natural range in the country where it is farmed. Of these countries, 111 have farmed at least 1 non-native species with 64 farming exclusively non-native species and 15 that farm only native species (Table 1). The whiteleg shrimp (Penaeus vannamei) is the most widely farmed species, cultivated across 54 countries (Table 2; Appendix S3). The signal crayfish has only been farmed in non-native countries whereas the giant mud crab (Scylla serrata) has been farmed only in native countries (Appendix S3). Out of the 63 farmed species, 22 are considered invasive worldwide impacting at least 77 countries (Table 1; Appendix S1 and S4). Here, we define invasive as actual or probable negative ecological or economic impact documented in at least one population worldwide. The red swamp and the spiny-cheek (Faxonius limosus) crayfishes are invasive in over 20 countries (Table 2). There are several pathways by which crustaceans have been shown to spread including ballast water, pet trade and hull fouling (Table 2). However, it is established that aquaculture is a major driver/pathway in invasion crustaceans with at least 19 of the 22 invasive species introduced through aquaculture (Table 2, Appendix S5), 14 of those affecting at least 30 countries (Table 1; Appendix S4). Causes of their introduction include unintentional escape (e.g. when used as fish food49), intentional release from crustacean aquaculture31, 51 or transfer through 'hitchhiking' on other species as was the case with the Chinese mitten crab (Eriocheir sinensis).42, 65, 66 It is important to note that these results are likely underestimated due to the incomplete reporting of both farming and invasions. Brine shrimp Artemia franciscana Blue crab Callinectes sapidus Native species Human activities (fishing, aquaculture)30 European shore crab Carcinus aestuarii Competition Predation33 European green crab Carcinus maenas Competition Predation Herbivory/grazing/browsing Interaction with other invasive species35, 36 Threat to or loss of native species: decline of native population (e.g., bivalves) Habitat disruption35 Altered trophic level Modified gene pool or selective loss of genotypes Ecosystem change or habitat alteration Modification of natural benthic communities Greater vulnerability to invasions Damaged ecosystem services Impact on agriculture, human health, livelihoods, aquaculture/fisheries36 Smooth marron Cherax cainii Competition Parasitism Disease transmission37, 38 Impact on native species Habitat alteration37, 38 Common yabby Cherax destructor Competition Predation Pest and disease transmission Herbivory/grazing/browsing39 Food web dynamic changes Habitat alteration Infrastructure damage Negative impact on agriculture Reduced native biodiversity Threat to or loss of endangered species Threat to or loss of native species39, 40 Red claw crayfish Cherax quadricarinatus Competition Predation9 Impact on native fauna: population decline, species replacement Trophic web alteration Ecosystem service disruption (fisheries, irrigation systems) Chinese mitten crab Eriocheir sinensis Competition Predation Aquaculture/fisheries: predation including target species for commercial (agriculture, aquaculture, fisheries) and recreational fishing Infrastructure damage: greater riverbank erosion and clogging of commercial water intake Damaged ecosystem services Impacts on human health, livelihoods Damaging aquatic food chain of freshwater and estuarine habitats Ecosystem change or habitat alteration: modification of hydrology Threat to or loss of native species42 Spinycheeck crayfish Faxonius limosus Competition Pest and disease transmission Herbivory/grazing/browsing Hybridization Predation43, 44 Threat to or loss of native species: reduced native biodiversity (native crayfish populations) Threat to or loss of endangered species Modified gene pool or selective loss of genotypes Impact on native habitats Impact on fish community Decreased food resources and thus mollusc and amphibian occurrences Altered trophic levels Greater vulnerability to invasions Modification of hydrology Modification of natural benthic communities Ecosystem change or habitat alteration Infrastructure damage (destabilized riverbanks) Damaged ecosystem services Negative impact on aquaculture/fisheries43, 44 Tahitian prawn Macrobrachium lar Tahitian prawn Macrobrachium nippponense Predation46 Competition47 Possible disease transmission48 Giant river prawn Macrobrachium rosenbergii Possible disease transmission Interbreeding with local species50 Brown shrimp Metapenaeus monoceros Signal crayfish Pacifastacus leniusculus Competition Pest and disease transmission Predation53-55 Modification of natural benthic communities Reduced native biodiversity Threat to or loss of native species (decline of native species Austropotamobius pallipes)55 Northern Brown Shrimp Penaeus aztecus Japanese king prawn Penaeus japonicus Tiger prawn Penaeus monodon Competition Herbivory Parasitism58, 59 Threatened native species Modification of natural benthic communities Modification of nutrient regime Impacts on aquaculture and fisheries Green tiger prawn Penaeus semisulcatus Whiteleg shrimp Penaeus vannamei Pest and disease transmission Competition for habitat and food59, 61 Modified gene pool or selective loss of genotypes Modification of natural benthic communities Modification of nutrient regime Negative impact on aquaculture/fisheries Threat to or loss of native species59 Narrow-clawed crayfish Pontastacus leptodactylus Blue swimmer crab Portunus pelagicus Competition Pest and disease transmission Predation63 Altered trophic level Modification of natural benthic communities Reduced native biodiversity Threat to or loss of native species63 Red swamp crayfish Procambarus clarkii Competition Predation on insects and molluscs Disease transmission64 Reduced resources available for native species (e.g. destruction of macrophytes). Human activities (infrastructure, agriculture). Ecosystem change or habitat alteration Human health Threat to or loss of native species64 These 22 invasive crustaceans farmed in aquaculture originate from diverse regions and environments including marine, brackish, and freshwater85 (Appendix S1). Their introductions into non-native regions have resulted to multiple and severe impacts (Table 2). For instance, the European green crab and Chinese mitten crab outcompete and prey on native species, leading to native population declines; consequently, they are listed among '100 of the worst invasive alien species'.67 Four of these 22 species are also listed on the European list of invasive alien species of concern, the spiny-cheek crayfish, the red swamp crayfish, the signal crayfish, and the Chinese mitten crab.68 The types of impacts and associated mechanisms of these invasive crustaceans are diverse (Table 2). Tiger prawn (Penaeus monodon) and red swamp crayfish are vectors of viral diseases such as the white spot syndrome baculovirus.69 Crayfish also transmit crayfish plague caused by the oomycete Aphanomyces astaci, listed among the 100 worst invasive alien species globally.67 Some crustaceans are considered ecosystem engineers15, 70 that can significantly impact the structure of invaded habitats, thereby affecting other species and altering ecosystem dynamics. The European green crab reduces eelgrass biomass by damaging rhizomes and plant shoots while burrowing for shelter and prey.71 Similarly, the red swamp crayfish alters water quality, increasing turbidity and reducing dissolved oxygen levels.72 These invasive crustaceans can also impact economic activities such as aquaculture, fisheries and agriculture.17 The burrowing behaviour of the common yabby (Cherax destructor) can jeopardize dam walls, thus affecting farmers.73 In Lake Naivasha, local fishermen estimated that the red swamp crayfish reduced their catch's food provisioning by up to 30% due to crayfish-induced damage to fishing nets.74 Thus, the risk on human activities results in massive economic consequences since four crabs— the blue crab, the European green crab (Carcinus maenas), the Chineese mitten crab and the blue swimmer crab (Portunus pelagicus)—and three crayfish species—the red swamp crayfish, the signal crayfish and the spiny-cheeck crayfish. —farmed in aquaculture rank among the costliest invasive crustaceans.17 Despite the acknowledged risks, there is still no global picture of the risk posed by farmed crustacean species in aquaculture. As a first step to address this gap, we propose a simple but widely applicable classification system based on two primary criteria: (1) the species documented global invasion history, and (2) whether the species is farmed outside its native regions. This system creates four possible outcomes, which we used to create a preliminary risk index ranging from limited risk (A) to high (D) (Figure 1). Species farmed in their native range are of low concern if escaped populations establish outside the farm (category A), but of medium concern if they are invasive in other (non-native) range (category B). Conversely, species farmed outside their native range and never reported as invasive (category C) have a high risk of becoming invasive if they escape and establish. The highest concern is for species farmed outside their native range and with a documented invasion history (category D). As a preliminary decision and in the absence of more in-depth risk assessments, we suggest applying appropriate management measures of the 63 farmed crustacean species based on their classification. Species with the lowest risk classifications (category A & B), which total 39 species, can continue to be farmed in their native regions, focusing biosecurity efforts on international transport. The seven species farmed in non-native countries (category C), require appropriate biosecurity and monitoring measures to prevent escapes from farms or transports. For the 17 species classified in the highest-risk category (D), farming in non-native regions must be avoided. Selecting species for aquaculture that minimize biological invasion risks while boosting economic potential is crucial. Therefore, it is essential to prioritize farming species within their native regions (A & B),10 particularly for open pond water farming. However, it is important to note that even native species can have detrimental impacts if released in large quantities.75 Farming species outside their native region may only be safe if not only species are reared in enclosed structures but also if current and future environmental conditions are unfavourable to their invasiveness. The current and future risks of establishment of non-native species can be predicted with tools such as species distribution models. Thus, conducting local or national spatial prediction analyses before establishing farms may allow the building of non-native farming while lowering the risk that species becomes invasive.76 Biosecurity and early response (following regular monitoring) are the most effective ways of managing non-native species.12, 77 The most basic approaches include: (i) farming sterile or unisex individuals, (ii) isolating farms with closed structures away from natural aquatic habitats, (iii) implementing clean-up protocols and special attire to prevent the spread of eggs and contaminants, (iv) using adequate equipment such as nets to prevent individual escape (e.g., through predation), including equipment maintenance to prevent long-term breakdowns and (v) regularly monitoring surrounding regions.78, 79 Risks are further reduced through tailored risk assessments20, 80, 81 and updating laws31 and regulations at different scales.20, 31, 82 For example, the four species in the European list of invasive alien species68 are forbidden to be farmed.83 We acknowledge that in many cases the long-term negative consequences of biological invasions may be disregarded because of the immediate social and economic benefits of aquaculture or a lack of awareness of the impacts. Our objective here was to highlight these consequences and promote responsible choices in aquaculture, such as selecting native species or implementing specific biosecurity measures, to collectively progress towards sustainable aquaculture with a reduced role in biological invasions. The classification we proposed serves this objective by informing about the risks posed by farmed aquaculture crustacean species. While based on current knowledge, it could be refined as more gaps in our understanding are addressed. Firstly, not all countries farming these crustaceans are currently present in the FAO dataset.24 Examples include Venezuela and Brazil which are not present in the FAO despite farming the tiger prawn, also invasive there.84 The efficient reporting of newly farmed species to the FAO dataset also varies, mostly by country. Secondly, there are species level gaps in the dataset, one example being the brine shrimp (Artemia franciscana) which is not included in FAO as of now. Additionally, the FAO often provides information at higher taxonomic levels such as genus or family, thus complicating the identification of all farmed crustaceans, including potentially invasive ones. For instance, the Metapenaeus genus may include one of two invasive alien species of this taxonomic group. Our study may also underestimate the extent of farms located in non-native regions due to uncertainties in the native regions of some species. This is a problem particularly acute in very large countries (e.g., Australia, Brazil, Russia, USA, China) where farming is reported at the national level, whereas a species is native to specific parts of the country. For example, the smooth marron (Cherax cainii) is native to parts of Australia but invasive in others. Further, delays in detecting invasive species in the wild and in quantifying their impact hinder our ability to categorize species as invasive accurately. Finally, information on unregistered or illegal farms is lacking,9 making it difficult to assign accurate risk categories to some species. Consequently, we cannot rely solely on this dataset to assign a risk category to a given species. Our classification is presented more to illustrate our proposal, enhance understanding of invasion risks related to farmed species crustacean species, assist in prioritizing containment strategies, and inform the selection of future farming locations and species. This approach is also relevant for other farmed aquatic groups like molluscs or fish. Eléna Manfrini: Conceptualization; investigation; methodology; validation; visualization; writing – review and editing; writing – original draft; formal analysis; project administration; data curation; resources. Franck Courchamp: Supervision; conceptualization; investigation; funding acquisition; methodology; validation; visualization; writing – review and editing; formal analysis; resources. Boris Leroy: Supervision; conceptualization; investigation; writing – original draft; writing – review and editing; visualization; validation; methodology; formal analysis; resources. This study received support from support from the AXA Research Fund Chair for Biological Invasions at the University of Paris Saclay. We express our gratitude to Gabriel Klippel for his assistance in reporting missing farmed species. We thank Clara Marino, Celine Bellard, Åsa Berggren, Antonín Kouba and Fran Oficialdegui for their invaluable and constructive comments on the manuscript. We thank Thomas Hughes for their assistance in revising the English style and grammar of this manuscript. We also thank three Reviewers and the Editor for helpful comments and suggestions which improved this manuscript. The data that supports the findings of this study are available in the supplementary material of this article. APPENDIX I. Invasive status and native regions of the 63 crustaceans farmed in aquaculture. The majority of native region were found on SeaLifeBase.85 APPENDIX II. Global distribution of the number of farmed crustaceans and invasive crustaceans farmed for aquaculture for the 22 invasive farmed species. The rectangles shown at the centre bottom of this schematic map represent the status of 43 regions (18 islands, 14 countries and 11 overseas territories) that are too small to be depicted. Blue countries are those with no records of farmed crustacean invasion. The large number of countries with purple, red or pink hues are those in which farmed species have become invasive because of aquaculture. Note that a species can be invasive in a country even if it is not farmed within its borders. Consequently, a country may have invasive species that exceed those farmed. APPENDIX III. Species farming countries and status (native or non-native) of the 63 crustaceans farmed in aquaculture. APPENDIX IV. Invaded countries of the 22 invasive crustaceans farmed in aquaculture. Countries where species are farmed and invasive are written in bold. APPENDIX V. Classification of the 63 crustacean species farmed in aquaculture. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.