Although it is technically more appropriate to refer to polychaetes as marine annelids (Hutchings & Kupriyanova, Reference Hutchings and Kupriyanova2018) we still use the term polychaetes due to its wide use in the historical literature. Polychaetes form one of the most important components of benthic communities, representing between 30 and 50% (but up to 70%) of the total abundance of the benthos (Rosenberg et al., Reference Rosenberg, Hellman and Lundberg1996; Witte et al., Reference Witte, Aberle, Sand and Wenzhöfer2003; Murugesan et al., Reference Murugesan, Muniasamy, Muthuvelu, Vijayalakshmi and Balasubramanian2011; Kuk-Dzul et al., Reference Kuk-Dzul, Gold-Bouchot and Ardisson2012). Polychaetes also comprise around half of the diversity of annelids with about 100 families and around 12,000 valid species (Appeltans et al., Reference Appeltans, Ahyong, Anderson, Angel, Artois, Bailly, Bamber, Barber, Bartsch, Berta, Błazewicz-Paszkowycz, Bock, Boxshall, Boyko, Brandão, Bray, Bruce, Cairns, Chan, Cheng, Collins, Cribb, Curini-Galletti, Dahdouh-Guebas, Davie, Dawson, De Clerck, Decock, De Grave, De Voogd, Domning, Emig, Erséus, Eschmeyer, Fauchald, Fautin, Feist, Fransen, Furuya, Garcia-Alvarez, Gerken, Gibson, Gittenberger, Gofas, Gómez-Daglio, Gordon, Guiry, Hernandez, Hoeksema, Hopcroft, Jaume, Kirk, Koedam, Koenemann, Kolb, Kristensen, Kroh, Lambert, Lazarus, Lemaitre, Longshaw, Lowry, MacPherson, Madin, Mah, Mapstone, McLaughlin, Mees, Meland, Messing, Mills, Molodtsova, Mooi, Neuhaus, Ng, Nielsen, Norenburg, Opresko, Osawa, Paulay, Perrin, Pilger, Poore, Pugh, Read, Reimer, Rius, Rocha, Saiz-Salinas, Scarabino, Schierwater, Schmidt-Rhaesa, Schnabel, Schotte, Schuchert, Schwabe, Segers, Self-Sullivan, Shenkar, Siegel, Sterrer, Stöhr, Swalla, Tasker, Thuesen, Timm, Todaro, Turon, Tyler, Uetz, Van Der Land, Vanhoorne, Van Ofwegen, Van Soest, Vanaverbeke, Walker-Smith, Walter, Warren, Williams, Wilson and Costello2012; Weigert & Bleidorn, Reference Weigert and Bleidorn2016; Magalhães et al., Reference Magalhães, Hutchings, Oceguera-Figeroa, Martin, Schemelz, Wetzel, Wiklund, Maciolek, Kawauchi and Williams2021). The majority of these families occur worldwide and are found in nearly every marine habitat where they often dominate macrofaunal assemblages (Hutchings, Reference Hutchings1998).
Polychaetes display a diverse range of life histories and feeding guilds (Fauchald & Jumars, Reference Fauchald and Jumars1979; Jumars et al., Reference Jumars, Dorgan and Lindsay2015) allowing them to occupy almost all trophic levels and, coupled with their distribution and abundance, they generally provide a whole suite of ecological functions and ecosystem services where they occur in their native ranges (Cyrino et al., Reference Cyrino, Coutinho, Teixeira, Simone and Santos2018). As such, they are often regarded as ecosystem engineers (Fadhullah & Syakir, Reference Fadhullah and Syakir2016), altering their surrounding environments through their ability to act as bioturbators, sediment stabilizers or refuge/substrate providers. Furthermore, some polychaetes are of practical use to humans as bioindicators of a range of pollutants (Mauri et al., Reference Mauri, Baraldi and Simonini2003; Giangrande et al., Reference Giangrande, Licciano and Musco2005; Catalano et al., Reference Catalano, Moltedo, Martuccio, Gastaldi, Virno-Lamberti, Lauria and Ausili2012; Maranho et al., Reference Maranho, Baena-Nogueras, Lara-Martín, DelValls and Martín-Díaz2014; Pires et al., Reference Pires, Almeida, Calisto, Schneider, Esteves, Wrona, Soares, Figueira and Freitas2016) as well as ecosystem health (Cardoso et al., Reference Cardoso, Bankovic, Raffaelli and Pardal2007).
The economic contributions of polychaetes are also substantial; in a global review of bait worm fisheries, Watson et al. (Reference Watson, Murray, Schaefer and Bonner2017) estimated that the ~121,000 tons of polychaetes collected globally were valued at £5.9 billion. They found that the five most expensive marine species sold on the global fisheries market (price kg−1) are all polychaetes. Further economic impacts are experienced when polychaetes act as pests, such as shell-boring spionids (Dipolydora spp., Polydora spp., Boccardia spp.) that have a long history of impacting shellfish aquaculture industries worldwide by devaluing products destined for the half-shell market and requiring burdensome treatments and interventions to manage infestations (Spencer et al., Reference Spencer, Martinelli, King, Crim, Blake, Lopes and Wood2020).
Globally, opportunities have increased for the transport of polychaetes beyond their native ranges to become aliens (synonyms: adventive, exotic, foreign, introduced, non-indigenous, non-native or neocosmopolitan) (Richardson et al., Reference Richardson, Pyšek, Carlton and Richardson2011; Blackburn et al., Reference Blackburn, Essl, Evans, Hulme, Jeschke, Kühn, Kumschick, Marková, Mrugała, Nentwig, Pergl, Pyšek, Rabitsch, Ricciardi, Richardson, Sendek, Vilà, Wilson, Winter, Genovesi and Bacher2014; Robinson et al., Reference Robinson, Alexander, Simon, Griffiths, Peters, Sibanda, Miza, Groenewald, Majiedt and Sink2016; Darling & Carlton, Reference Darling and Carlton2018). It has been estimated that there may be as many as 300 alien polychaete species in various regions of the world (Çinar, Reference Çinar2013). However, this number needs to be revised, as some species previously considered to be ‘cosmopolitan’ are confirmed as aliens (e.g. Bergamo et al., Reference Bergamo, Carrerette and Nogueira2019), as cryptic invasions are uncovered (e.g. Elgetany et al., Reference Elgetany, van Rensburg, Hektoen, Matthee, Budaeva, Simon and Struck2020), or as species previously thought to be alien resolve into multiple indigenous species (Simon et al., Reference Simon, van Niekerk, Burghardt, Ten Hove and Kupriyanova2019). The deliberate distribution of polychaetes via the trade of bait worms can inadvertently lead to their dispersal and establishment when live unused bait is discarded, as occurred in Portugal with the importation of Perinereis aibuhitensis from Korea (Fidalgo E Costa et al., Reference Fidalgo E Costa, Gil, Passos, Pereira, Melo, Batista, Cancela da Fonseca, Sarda, San Martín, Lopez, Martín and George2006). Furthermore, Mito & Uesugi (Reference Mito and Uesugi2004) showed that out of the 620 million live animals imported into Japan in 2003, 90% were classified as worms for fishing bait, suggesting a great scope for spread of worms via this vector. The global trade of molluscs such as oysters, mussels and abalone is considered one of the most important vectors of alien species (Ruesink et al., Reference Ruesink, Lenihan, Trimble, Heiman, Micheli, Byers and Kay2005) including shell-boring worms such as Boccardia proboscidea (Simon et al., Reference Simon, Thornhill, Oyarzun and Halanych2009; Simon & Sato-Okoshi, Reference Simon and Sato-Okoshi2015). Worms may also be spread unintentionally when fouling polychaetes such as Ficopomatus enigmaticus, Hydroides elegans and Sabella spallanzanii travel the world on ship hulls (Vitousek et al., Reference Vitousek, D'Antonio, Loope, Rejmánek and Westbrooks1997; Kocak et al., Reference Kocak, Ergen and Çinar1999; Hayes et al., Reference Hayes, Cannon, Neil and Inglis2005). Furthermore, with the increased speed of shipping, trans-oceanic shipping can now take place in less time than the duration of larval stages of most marine invertebrates. Thus, the huge volumes of ballast water carried by these ships and dumped in or near ports have also led to the establishment of invasive species (Carlton & Geller, Reference Carlton and Geller1993; Çinar, Reference Çinar2013).
Once established in recipient regions, alien species may cause significant changes to local species richness and abundance, population genetic composition, behaviour patterns, trophic networks, ecosystem productivity or habitat structure through competition, displacement or predation (Brooks et al., Reference Brooks, D'Antonio, Richardson, Grace, Keeley, Ditomaso, Hobbs, Pellant and Pyke2004; Hendrix et al., Reference Hendrix, Callaham, Drake, Huang, James, Snyder and Zhang2008; Shine, Reference Shine2010; Pyšek et al., Reference Pyšek, Jarošík, Hulme, Pergl, Hejda, Schaffner and Vilà2012; Ricciardi et al., Reference Ricciardi, Hoopes, Marchetti and Lockwood2013). There has therefore been significant interest in evaluating the impacts of alien species in different components of recipient ecosystems (Blackburn et al., Reference Blackburn, Essl, Evans, Hulme, Jeschke, Kühn, Kumschick, Marková, Mrugała, Nentwig, Pergl, Pyšek, Rabitsch, Ricciardi, Richardson, Sendek, Vilà, Wilson, Winter, Genovesi and Bacher2014; Bacher et al., Reference Bacher, Blackburn, Essl, Genovesi, Heikkilä, Jeschke, Jones, Keller, Kenis, Kueffer, Martinou, Nentwig, Pergl, Pyšek, Rabitsch, Richardson, Roy, Saul, Scalera, Vilà, Wilson and Kumschick2018; Pyšek et al., Reference Pyšek, Hulme, Simberloff, Bacher, Blackburn, Carlton, Dawson, Essl, Foxcroft, Genovesi, Jeschke, Kühn, Liebhold, Mandrak, Meyerson, Pauchard, Pergl, Roy, Seebens, Kleunen, Vilà, Wingfield and Richardson2020). Unfortunately, marine invasion science can be biased towards certain taxonomic groups, study types, marine systems and invasion stages. For example, South African marine invasion science is biased towards conducting field surveys on established species, especially Mytilus galloprovincialis, in the rocky intertidal (Alexander et al., Reference Alexander, Simon, Griffiths, Peters, Sibanda, Miza, Groenewald, Majiedt, Sink and Robinson2016), while impacts of the movement of oysters have also been reviewed extensively (e.g. Haupt et al., Reference Haupt, Griffiths, Robinson and Tonin2010).
Few studies have been conducted on the impacts of alien polychaetes in their recipient regions (Schwindt et al., Reference Schwindt, Bortolus and Iribarne2001; Holloway & Keough, Reference Holloway and Keough2002a; Delefosse et al., Reference Delefosse, Banta, Canal-Vergés, Penha-Lopes, Quintana, Valdemarsen and Kristensen2012; Elías et al., Reference Elías, Jaubet, Llanos, Sanchez, Rivero, Garaffo and Sandrini-Neto2015). However, because many polychaetes provide ecosystem functions in their natural distribution ranges, it is likely that they may have significant impacts should the worms become established as aliens. An ecological function such as bioturbation comprises a series of processes that affects the physical and chemical properties of the sediment that may strongly influence bacterial communities involved in nutrient cycling (Biles et al., Reference Biles, Paterson, Ford, Solan and Raffaelli2002), ultimately modifying the benthic community structure. For example, bioturbators, such as the deposit-feeding lugworm family Arenicolidae, have been known to exclude sympatric species such as the tube-building polychaetes Polydora cornuta and Lanice conchilega (Volkenborn et al., Reference Volkenborn, Robertson and Reise2009). Tube-building polychaetes, conversely, are sediment stabilizers which can aid in protecting the environment against erosion (Frey & Wheatcroft, Reference Frey and Wheatcroft1989), and facilitate the establishment of many other species not only by providing attachment points for plants and bivalves but also by providing refugia for smaller infaunal organisms, leading to higher species diversities in areas where they are found (Bell & Coen, Reference Bell and Coen1982; Ban & Nelson, Reference Ban and Nelson1987). Finally, abundant soft-bottom polychaetes have also been known to play a major role in the diets of demersal fish (Yeung et al., Reference Yeung, Yang, Jewett and Naidu2013) and birds (Kalejta & Hockey, Reference Kalejta and Hockey1991).
Understanding the impacts of alien polychaetes at species level is crucial due to the great variations in morphology, feeding modes and reproductive cycles of polychaetes as well as the services that they provide and their abundance.
A review of the impacts that alien polychaetes are having worldwide could help predict future alien establishments and thereby facilitate management of new alien species. However, impacts at species level are context dependent and impacts ascertained for one species may not be indicative of the expected impacts of closely related species or sometimes even for the same species in a different ecosystem. Indeed, some species behave differently outside their native distribution range as in the case of B. proboscidea, a non-reef forming species native to California that builds massive intertidal reefs in sewage-impacted areas in the South-west Atlantic, causing a reduction in the diversity of native species (Jaubet et al., Reference Jaubet, Sánchez, Rivero, Garaffo, Vallarino and Elías2011; Elías et al., Reference Elías, Jaubet, Llanos, Sanchez, Rivero, Garaffo and Sandrini-Neto2015). Furthermore, this species is a pest on abalone farms in South Africa (Simon et al., Reference Simon, Worsfold, Lange and Sterley2010) but not in its native distribution. A review of species impacts can therefore help alert managers to unpredictable species such as B. proboscidea and even help point to local gaps in knowledge by highlighting overlooked study types or marine systems.
Information about the impact of alien polychaete species is sparse or restricted to some geographic areas and species (Çinar, Reference Çinar2013; Katsanevakis et al., Reference Katsanevakis, Wallentinus, Zenetos, Leppäkoski, Çinar, Oztürk, Grabowski, Golani and Cardoso2014), and to date there has been no integrative and systematic review of the status and gaps of knowledge on this topic. The present systematic review analysed the advances in the research on the impacts of alien polychaetes in marine ecosystems and identifies gaps in the present knowledge that can be used to inform future research. This review aims to answer the following specific questions:
(1) How many and which alien polychaete species have been investigated globally to measure their impact?
(2) What are the trends in research into the impacts of alien polychaetes in marine ecosystems?
(3) What kinds of impacts do alien polychaetes have?
(4) What are the different management strategies that have been proposed or executed to manage different scenarios of impacts in the environment?
Materials and methods
This systematic review was performed using the main principles of the PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) approach, which recommends a series of procedures for systematic reviews and meta-analyses to make them repeatable and prevent low-quality or methodologically biased studies (Moher et al., Reference Moher, Liberati, Tetzlaff and Altman2009; Sierra-Correa & Cantera Kintz, Reference Sierra-Correa and Cantera Kintz2015). The approach consists of four phases: (1) Identification of publications through the systematic use of search engines; (2) Screening publications based on titles, abstracts and keywords; (3) Judging eligibility after a full review of remaining publications; and (4) Inclusion of all publications remaining in the final subset to extract the information (Figure 1).
Data collection and eligibility criteria
The bibliographic search focused on peer-reviewed publications in English from reputable journals with research conducted in marine environments. We followed the recommendations of Koricheva et al. (Reference Koricheva, Gurevitch and Mengersen2013) and the search was conducted using both the advanced systematic search engine in Elsevier's Scopus database (www.scopus.com) and ISI Web of Science (www.webofknowledge.com).
The criteria for selection included any article, review or book chapter published between 1950 and 31 December 2020, with the following search terms in the title, abstract or keywords:
(1) ‘impact’, OR ‘impacts’ OR ‘effect’ OR ‘effects’
(2) ‘alien species’, OR ‘invasive species’, OR ‘allochthonous species’, OR ‘introduced species’ OR ‘non-indigenous species’ OR ‘non-native species’ OR ‘invasion’ OR ‘exotic’ OR ‘adventive’ OR ‘foreign’
(3) ‘polychaetes’ OR ‘polychaeta’ OR ‘marine worm’ OR ‘marine worms’.
The following information was extracted from each selected article:
(1) Year of publication.
(2) Marine system: aquaculture facility, coastal lagoon, estuary, harbour, marina, open coast, or multiple if the study included more than one type of marine system.
(3) Study type: Field survey, experiment in situ, field and laboratory experiment, laboratory experiment, review, theoretical model and meta-analysis.
(4) Family of polychaetes.
(5) Species of polychaetes.
(6) Impact of alien species, according to the classification of Blackburn et al. (Reference Blackburn, Essl, Evans, Hulme, Jeschke, Kühn, Kumschick, Marková, Mrugała, Nentwig, Pergl, Pyšek, Rabitsch, Ricciardi, Richardson, Sendek, Vilà, Wilson, Winter, Genovesi and Bacher2014).
A field survey refers to research conducted during a sampling survey followed by analysis of samples in the laboratory; an experiment in situ was conducted in the field followed by analysis of samples in the laboratory; field and laboratory experiment is a combination of these two study types in the same research; theoretical model refers to studies that analysed data to design a mathematical model; meta-analyses is any research that applied statistical analysis that combined the results of multiple scientific studies; a review is any research based on the revision of the literature of invasive taxa that included one or more species of marine annelids.
All species names and authorities were verified and updated according to the online World Polychaeta Database (Read & Fauchald, Reference Read and Fauchald2021).
The impacts of alien polychaete species were evaluated according to the classification of alien species proposed by Blackburn et al. (Reference Blackburn, Essl, Evans, Hulme, Jeschke, Kühn, Kumschick, Marková, Mrugała, Nentwig, Pergl, Pyšek, Rabitsch, Ricciardi, Richardson, Sendek, Vilà, Wilson, Winter, Genovesi and Bacher2014). This classification system is based on the magnitude of the environmental impacts with regards to the impact mechanism (IMo) used to code species in the International Union for Conservation of Nature (IUCN) Global Invasive Database (Table 1). This system uses five semi-quantitative scenarios for each IMo, so impact values range from one to five, where one is minimal impact and five the highest impact that could be documented in 13 impact mechanisms (Table 1). Thus, the classification considers consequences not likelihoods, so species are classified on the basis of the evidence of all their most severe documented impacts in regions to which they have been introduced (Blackburn et al., Reference Blackburn, Essl, Evans, Hulme, Jeschke, Kühn, Kumschick, Marková, Mrugała, Nentwig, Pergl, Pyšek, Rabitsch, Ricciardi, Richardson, Sendek, Vilà, Wilson, Winter, Genovesi and Bacher2014).
The impact classes are according to the impact mechanisms (IMos) in the GISD (Global Invasive Species Database).
The Identification phase produced 885 papers (Figure 1). Nine additional papers relevant to the topic, which were independently identified by the authors during the review process, were added to bring the total to 894 papers. Duplicates accounted for 238 of these records and after removal left 656 papers. During the Screening phase, based on the revision of the title, abstract and keywords, we removed a further 470 records which did not include information relevant to the impact of alien marine polychaetes, resulting in 186 papers remaining. Finally, in the Eligibility phase, the full texts were evaluated, and 36 papers were excluded for not including relevant information about any impacts of alien polychaete species (Figure 1). Thus, 150 papers remained to be included in this study. The bibliographic details of all papers are available in Supplementary Material (Supplementary Table S1).
Annual trend of papers published
The final subset of papers spanned the period from 1980 to 31 December 2020. Only six papers were published on the impacts of alien polychaetes in the 17 years from 1980 to 1997. Thereafter, research on the topic increased until averaging almost six papers annually between 1998 and 2020, reaching a maximum of 12 papers published in both 2018 and 2020 (Figure 2).
As time went by, there was a change in both the systems investigated and the types of studies conducted. In the initial period between 1980 and 1997, the marine systems studied were limited to coastal lagoons, estuaries and marinas, after which aquaculture facilities, open coasts and marine harbour systems also featured (Figure 3). Only from 2002 onwards were papers focusing on multiple marine systems within a single paper published (Figure 3). Over the complete timespan, 54 papers (36%) reported on research conducted on open coasts (Figure 4) followed by 27 (18%) studies in coastal lagoons, 19 (13%) in estuaries, 18 (12%) in harbours and 16 (10%) in multiple systems (Figure 4). The fewest studies were conducted in aquaculture facilities and marinas which accounted for 9 (6%) and 7 (5%) studies, respectively.
Study types in the period 1980–1997 were mainly field surveys with results of only one field and laboratory experiment published in that period (Davies et al., Reference Davies, Stuart and de Villiers1989) (Figure 5). From 1998 onwards, field surveys remained popular but several other study types also rose in popularity (Figure 5). The breakdown of study types over the complete period shows field surveys as the most popular with 70 papers (46%), followed by in situ experiments with 25 papers (17%), 23 review papers (15%), 18 laboratory experiments (12%) and 10 theoretical studies (7%) (Figure 6). Only three studies included both field and laboratory experiments (2%) and only one meta-analysis (<1%) has been conducted.
Six papers were excluded (Rodriguez, Reference Rodriguez2006; Levin & Crooks, Reference Levin, Crooks, Wolanski and McLusky2011; Olenin & Minchin, Reference Olenin, Minchin, Wolanski and McLusky2011; Çinar, Reference Çinar2013; Anton et al., Reference Anton, Geraldi, Lovelock, Apostolaki, Bennett, Cebrian, Krause-Jensen, Marbà, Martinetto, Pandolfi, Santana-Garcon and Duarte2019; Bruschetti, Reference Bruschetti2019) from the analysis of geographic distribution of research. These papers were global reviews and one meta-analysis not investigating any specific geographic region. The remaining 144 papers were spread among 18 regions around the world (Figure 7). Half the papers were based on research conducted in two regions: the Baltic (33%) and South-west Atlantic (17%). Other well-studied geographic regions included the Mediterranean, the US Pacific coast and Australia, contributing just under 30% more of the papers. In contrast, less well-studied regions included the Wadden Sea (7 papers, 5%), South Africa (5 papers, 3%), New Zealand (4 papers, 3%) and the English Channel (3 papers, 2%). The remaining geographic regions represented were the Arabian Sea, Black Sea, Caspian Sea, Pacific coast of Canada, Sea of Azov, South-eastern Pacific, Tropical Eastern Pacific, U.S. Atlantic coast and Yellow Sea, each with a single publication.
In 11 of the 18 geographic regions studied around the world, more than one type of marine system has been studied (Figure 8). In the Baltic Sea most of the systems were studied (6 systems), except aquaculture facilities, followed by Australia and U.S. Pacific (5 each); Mediterranean and South Africa (4 each); South-west Atlantic, English Channel and Wadden Sea (3 each) and U.S. Atlantic coast, South-eastern Pacific and New Zealand (2 each) (Figure 8). In the South-west Atlantic, the main marine system studied was the coastal lagoon, followed by open coast and multiple systems, respectively. In the Mediterranean Sea, the papers focused mainly on harbours and open coasts, and fewer on aquaculture facilities and multiple systems. Studies from the Pacific coast of the USA mainly focused on aquaculture facilities and estuaries and in lower number harbours, marinas and open coast. In Australia, all marine systems were studied except aquaculture facilities and coastal lagoons.
The most common type of study was the field survey (conducted in all regions), followed by experiments in situ (7 regions), reviews (6 regions) and theoretical models (5 regions), whereas laboratory experiments and studies that included field and laboratory experiments were conducted in the fewest regions (Figure 9). The regions where all or most study types classified in the present review were conducted were the Baltic Sea, South-west Atlantic and the Pacific coast of the USA (Figure 9).
Number of species
The publications considered here provided information on impacts of 40 alien polychaete species, belonging to 11 families and 25 genera (Table 2, see Supplementary Table S1). In the present review 9 species were labelled as cryptogenic [CG] (see below) because their alien statuses are in question.
[CG], Cryptogenic species.
The superscript number indicates the number of publications that included information about the impact of the species. Species with more than 10 papers are indicated in bold.
The references are indicated with the numbers that appear in the supplementary material, Table S1.
The families with most species are Spionidae, Serpulidae, Sabellidae and Nereididae, together representing 83% of the total number of alien species investigated (Figure 10). The remaining 17% were represented by the families Capitellidae, Ampharetidae, Cirratulidae, Glyceridae, Maldanidae, Sternaspidae and Terebellidae.
The species investigated most intensely was the serpulid Ficopomatus enigmaticus with studies conducted in the South-west Atlantic, Atlantic and Pacific coast of the USA, South Africa, Black Sea and English Channel (Table 2). The second most studied species was the spionid Marenzelleria viridis, with its impacts analysed in the Baltic and Wadden Seas. A smaller number of papers also analysed the impact of Marenzelleria arctia and Marenzelleria neglecta in the Baltic Sea. Furthermore, several papers report the impact of Marenzelleria as a complex of these three species (Marenzelleria spp.) and additional studies referred to M. cf. arctia and M. cf. viridis. Thus, if studies of impact are considered at genus level, Marenzelleria would be the most studied genus in the world. However, it is important to note that almost all studies on this genus are concentrated in the Baltic Sea region while F. enigmaticus was studied in several geographic areas worldwide.
The species with the third highest number of publications was the Mediterranean sabellid Sabella spallanzanii, for which all studies were conducted in Australia and New Zealand. The spionid Boccardia proboscidea was the fourth species with most of the studies conducted in South-west Atlantic and South Africa.
Approximately 50% of the remaining 34 species studied globally have been investigated in at least one locality in the Mediterranean Sea, while investigations of the rest were conducted at various locations around the world, with only one paper each.
Impact of alien polychaete species
Reviews and meta-analyses were excluded from the analysis of impacts of alien polychaete species to avoid duplicating information. Following the Blackburn et al. (Reference Blackburn, Essl, Evans, Hulme, Jeschke, Kühn, Kumschick, Marková, Mrugała, Nentwig, Pergl, Pyšek, Rabitsch, Ricciardi, Richardson, Sendek, Vilà, Wilson, Winter, Genovesi and Bacher2014) classification, we applied the precautionary principle that cryptogenic species are evaluated as if they are aliens, but their impact categorization is modified by the [CG] label. This indicates that it is unclear if the species registered at a location is native or alien, or if the identification is questionable, as is the case for F. enigmaticus, Hydroides dianthus, Hydroides operculata, Branchiomma boholense, Branchiomma bairdi, Spirobranchus kraussii, Pseudopolydora paucibranchiata and Allita succinea. Although there is no doubt about the presence of Polydora websteri in the studies analysed in the present review (Martinelli et al., Reference Martinelli, Lopes, Hauser, Jimenez-Hidalgo, King, Padilla-Gamiño, Rawson, Spencer, Williams and Wood2020; Spencer et al., Reference Spencer, Martinelli, King, Crim, Blake, Lopes and Wood2020; Waser et al., Reference Waser, Lackschewitz, Knol, Reise, Wegner and Thieltges2020), its presence must be corroborated in other regions. The species studied in the publications analysed in this review could be assigned to 8 of the 12 impact mechanisms (IMo) defined by Blackburn et al. (Reference Blackburn, Essl, Evans, Hulme, Jeschke, Kühn, Kumschick, Marková, Mrugała, Nentwig, Pergl, Pyšek, Rabitsch, Ricciardi, Richardson, Sendek, Vilà, Wilson, Winter, Genovesi and Bacher2014) (Table 1; Figure 11): competition (1), transmission of diseases to native species (4), parasitism (5), biofouling (7), chemical (9), physical (10), structural (11) and interaction with other alien species (12). In general, most of the species studied in the publications analysed here were classified as having chemical, physical or structural impacts (IMo 11,10 and 9) in the ecosystem in the recipient region (Figure 11). Furthermore, 74% of the impacts could be classified as major or massive.
In the case of the spionid species that typically are part of the infauna (Marenzelleria species, Streblospio gynobranchiata, Streblospio benedicti, P. paucibranchiata, Polydora cornuta and Boccardia tricuspa) it was found that they mainly registered IMos in chemical, physical and structural categories with some cases of competition. Species that are shell borers (P. websteri, Polydora rickettsi, Polydora hoplura and Boccardia pseudonatrix) were classified with IMos of competition, parasitism and interaction with other alien species. The only species that registered a score in competition and parasitism as well in physical and structural impact in the ecosystem was B. proboscidea (Figure 11). In the case of Serpulidae species (reef builders), these registered mainly IMos in physical and structural impact on the ecosystem, additionally F. enigmaticus registered impact in transmission of diseases and interaction with other alien species, being the serpulid with most IMos. The IMo of biofouling was only registered in Hydroides elegans, Hydroides dirampha and Neodexiospira brasiliensis.
For the species of Sabellidae (tube dwellers) S. spallanzanii registered the most IMos: biofouling, chemical, physical and structural impact; Desdemona ornata and B. bairdi displayed physical and/or structural impacts; B. boholense registered a competitive impact mechanism and Terebrasabella heterouncinata was the only sabellid registering a parasitism IMo.
The remaining species (representatives of infauna) were assigned to Imos of structural impact on ecosystem, except for Perinereis linea assigned to IMo of transmission of diseases to native species and Clymenella torquata to IMo of interaction with other alien species.
Before the 1980s, many researchers accepted that globally widespread species, or cosmopolitanism, was common among polychaetes (Hutchings & Kupriyanova, Reference Hutchings and Kupriyanova2018). However, recent taxonomic revisions have shown that most species that are truly widespread, including polychaetes, have been spread by anthropogenic means (Darling & Carlton, Reference Darling and Carlton2018). It is therefore not surprising that the appearance and gradual increase in investigations into the impact of alien species coincided with this change in mind-set regarding ‘cosmopolitan’ vs alien species. Consequently, for this review, only papers published from 1980 onwards could be found that investigated impacts of alien polychaete species. Nevertheless, studies investigating the impacts of alien polychaete are scarce.
Development of alien impact research
When we analysed the development of research in the three most studied alien polychaete species, the first records of impacts were documented in the 1980s for the serpulid Ficopomatus enigmaticus on the Atlantic coast of the USA (Hoagland & Turner, Reference Hoagland and Turner1980) and the spionid Marenzelleria viridis (Essink & Kleef, Reference Essink and Kleef1988) in the Wadden Sea, while the first record for the sabellid Sabella spallanzanii was in the 1990s (Cohen et al., Reference Cohen, Currie and McArthur2000) in Australia.
The detection of F. enigmaticus on the Atlantic coast of the USA was possible due to the implementation of an extended study that monitored marine boring and fouling organisms in the vicinity of Barnegat Bay, New Jersey since 1971 (Hoagland & Turner, Reference Hoagland and Turner1980). Although the impact of this species has been assessed in several regions of the world, approximately a third of these studies (mainly experiments in situ and field surveys) have been conducted in the Mar Chiquita coastal lagoon of the South-west Atlantic (Supplementary Table S1). It is important to indicate that in this lagoon, F. enigmaticus was first reported in the early 1970s (Orensanz & Estivariz, Reference Orensanz and Estivariz1971), but papers investigating its impact only started being published 30 years later.
Studies on the impacts of M. viridis began with more field surveys and reviews, although publications of laboratory experiments, to evaluate the impact of this species mainly in the Baltic Sea region, started in 2003 (Kotta & Ólafsson, Reference Kotta and Ólafsson2003).
With regards to S. spallanzanii, there is evidence that this species has been present in Australia since at least 1965 (Hutchings, Reference Hutchings1999), however, we only found papers on the impact of this species in Australia (mainly experiments in situ) starting in the late 1990s (Cohen et al., Reference Cohen, Currie and McArthur2000). Meanwhile, in New Zealand, S. spallanzanii was detected by a national surveillance programme in 2008 (Read et al., Reference Read, Inglis, Stratford and Ahyong2011) but papers related to the impact of this species included a theoretical model, two experiments in situ and one field survey, in the period 2018–2020 (Supplementary Table S1).
The number of publications, types of research and timing of the research seem to be related to the implementation of monitoring programmes of estuaries and coastal areas and groups of research in some regions of the world. For example, the National Danish Aquatic Monitoring and Assessment Programme has been operating since the late 1980s in areas of the Wadden Sea, North Sea and Baltic Sea (Svendsen et al., Reference Svendsen, van der Bijl and Norup2005). The Baltic Sea, in particular, has an over 50-year-long tradition of monitoring soft-bottom macrofaunal communities, providing a unique time series to study changes over time (Nygård et al., Reference Nygård, Lindegarth, Darr, Dinesen, Eigaard and Lips2020). This tradition was reinforced with the Helsinki Commission (HELCOM) Baltic Sea Action Plan, adopted in 2007 by the coastal countries of the Baltic Sea (Denmark, Estonia, Finland, Germany, Latvia, Lithuania, Poland, Russia, Sweden as well as the European Community) which is structured around a set of ecological objectives used to define indicators and targets that include a regional monitoring implementation (Backer et al., Reference Backer, Leppänen, Brusendorff, Forsius, Stankiewicz, Mehtonen, Pyhälä, Laamanen, Paulomäki, Vlasov and Haaranen2010). In the South-west Atlantic, the presence and continuous activity of research groups has focused on benthic communities in institutions such as Universidad Nacional de Mar del Plata in Argentina. Here, researchers Rodolfo Elias, Maria Cielo Bazterrica, Maria L. Jaubet, Griselda V. Garaffo and Carlos Martin Bruschetti determined that in the last 50 years, changes in the community structure were induced by sewage discharge and introduction of non-indigenous species (Llanos et al., Reference Llanos, Jaubet and Elías2019; Martinez et al., Reference Martinez, Bazterrica and Hidalgo2020). In Australia research groups lead by the polychaete taxonomists Pat Hutchings, Elena Kupriyanova and Christopher J. Glasby are active at national museums of the country, while in New Zealand the research by Geoffrey Read at the National Institute of Water and Atmospheric Research is active in the taxonomy of polychaetes. In these last two countries the polychaete taxonomists collaborate with institutions and are involved in programmes in biosecurity such as the Center for Introduced Marine Pests (CRIMP) established by Australia in the early 1990s and the Biosecurity Act of 1993 in New Zealand which provides for targeted surveillance in harbours, ports, marinas and high-value natural environments (Atalah et al., Reference Atalah, Floerl, Pochon, Townsend, Tait and Lohrer2019).
Contrastingly, we found little information about the impact of alien polychaete species in the rest of coastal Europe except for the Mediterranean and Baltic Sea. This could be because the European Water Framework Directive (WFD) did not refer explicitly to alien species; this omission was rectified for the marine environment in the enactment of the Marine Strategy Framework Directive (MSFD). Unfortunately, countries in Europe are inconsistent in their use of historical dates to determine when a species is considered alien and few countries monitor alien species specifically for the WFD (Lehtiniemi et al., Reference Lehtiniemi, Ojaveer, David, Galil, Gollasch, McKenzie, Minchin, Occhipinti-Ambrogi, Olenin and Pederson2015; Boon et al., Reference Boon, Clarke and Copp2020). However, there are efforts to create lists of alien marine species which include polychaetes in Europe (Katsanevakis et al., Reference Katsanevakis, Wallentinus, Zenetos, Leppäkoski, Çinar, Oztürk, Grabowski, Golani and Cardoso2014) and specifically in the Mediterranean (Streftaris & Zenetos, Reference Streftaris and Zenetos2006; Zenetos, Reference Zenetos2010; Gerovasileiou et al., Reference Gerovasileiou, Voultsiadou, Issaris and Zenetos2016; Zenetos et al., Reference Zenetos, Çinar, Crocetta, Golani, Rosso, Servello, Shenkar, Turon and Verlaque2017), where the alien status of several species is questionable. With respect to the creation of lists of alien marine species, Marchini et al. (Reference Marchini, Galil and Occhipinti-Ambrogi2015) point out the importance of ‘best practices’ to standardize lists of marine alien species to avoid uncertainty in the species' taxonomic identification or the occurrence of the species in a specific area that will consequently determine its status as an alien. The implementation of monitoring programmes and ‘best practices’ in the development and elaboration of lists of marine alien species in different regions of the world will undoubtedly help in the development of the study field regarding impacts of alien polychaete species.
In general, except for papers that focus on F. enigmaticus, M. viridis and S. spallanzanii, most of the remaining papers about the impact of alien polychaete species have been field surveys. The least frequently conducted study types were field and laboratory experiments and meta-analyses, probably because conducting the former is logistically complicated, while too few data about impacts are available to conduct meaningful meta-analyses. However, the paucity of these study types are linked, because experiments are key in the generation of quantitative data to determine whether or not alien species are causing statistically significant alterations in an environment (Olenin & Minchin, Reference Olenin, Minchin, Wolanski and McLusky2011).
The least studied systems are marinas and aquaculture facilities, even though they are focal points of entry for alien species (Peters et al., Reference Peters, Griffiths and Robinson2014; Simon & Sato-Okoshi, Reference Simon and Sato-Okoshi2015). But as artificial environments, evaluating impact there is likely more complex. Furthermore, although the presence of shell-boring polychaete species on mariculture farms has been well documented (Sato-Okoshi et al., Reference Sato-Okoshi, Okoshi and Shaw2008; Simon & Sato-Okoshi, Reference Simon and Sato-Okoshi2015; Spencer et al., Reference Spencer, Martinelli, King, Crim, Blake, Lopes and Wood2020), problems with regards to the reliable identification of these species (if they are even identified to species level) has hindered the process of associating these impacts to alien or indigenous species (as discussed in more detail below). This, in turn, could have led many such studies from aquaculture facilities being overlooked by this review due to our search terms focusing on alien-orientated keywords. However, mariculture studies have rarely investigated the impacts of focal species outside studied mariculture farms (e.g. Culver & Kuris, Reference Culver and Kuris2000; Kuris, Reference Kuris2002) or have only identified to genus (Stenton-Dozey et al., Reference Stenton-Dozey, Jackson and Busby1999), probably including indigenous and alien species.
Impact of alien species
As mentioned previously, there is a lag between first detection of alien species and the first studies on impact. According to Blackburn et al. (Reference Blackburn, Lockwood and Cassey2015) the process whereby a species becomes an alien can be divided into the sequential stages of transport, introduction, establishment and spread. In the species analysed in this review, most of the IMos were classified as ‘massive’, which seems to reflect that alien polychaete species are probably only studied once significant impacts in the ecosystem have been noticed during establishment and spread stages in the ecosystem. The impacts of species reviewed here are strongly related to their biology and lifestyles and depends on whether the species build conspicuous reefs, are tube-dwellers, shell-borers or are part of the infauna.
Tube/reef building species
The serpulid F. enigmaticus is a calcareous tube builder that is 6–12 mm long (Fauvel, Reference Fauvel1923), and is considered an ecosystem engineer, as it may directly or indirectly control the availability of resources to other organisms by changing the physical state of biotic or abiotic materials (Jones et al., Reference Jones, Lawton and Shachak1994). This species, particularly in Mar Chiquita Lagoon in Argentina, builds intertidal calcareous reefs that grow up to 7 m in diameter and 0.5 m in height (Obenat & Pezzani, Reference Obenat and Pezzani1994) that have been expanding along this lagoon since 1975 until it covered 80% of this ecosystem (Schwindt & Iribarne, Reference Schwindt and Iribarne2000). These reefs have influenced many physical effects including the transport of sediments and flow of water (Schwindt et al., Reference Schwindt, Iribarne and Isla2004). The ongoing investigation of these reefs has made it possible to determine the cascading effects of this species and its influence in several ecological aspects such as changes in the community structure of native benthic communities (Schwindt et al., Reference Schwindt, Bortolus and Iribarne2001) and the effects of suspension feeding and biodeposition (Bruschetti et al., Reference Bruschetti, Bazterrica, Fanjul, Luppi and Iribarne2011). The suspension feeding activity of F. enigmaticus affects the composition of phytoplankton (Pan & Marcoval, Reference Pan and Marcoval2014) and zooplankton (Bruschetti et al., Reference Bruschetti, Luppi and Iribarne2016) and could be seen as a positive impact in some areas where it is introduced, because it contributes to maintaining water quality in polluted systems (Davies et al., Reference Davies, Stuart and de Villiers1989). Other positive aspects observed have been the increase of feeding and resting areas for migratory and local birds (Bruschetti et al., Reference Bruschetti, Bazterrica, Luppi and Iribarne2009), and the interaction with native macroalgae (Polysiphonia subtilissima) in a mutually beneficial relationship in the establishment of both species (Bazterrica et al., Reference Bazterrica, Bruschetti, Alvarez, Iribarne and Botto2014).
However, other aspects that are considered as negatives is that F. enigmaticus could be an intermediary in the transmission of parasites (Etchegoin et al., Reference Etchegoin, Merlo and Parietti2012), and facilitates the spread of other alien species (Bazterrica et al., Reference Bazterrica, Barón, Álvarez and Obenat2020). Another negative aspect of serpulid alien species F. enigmaticus is the dense encrustations on artificial substrates such as concrete marine facilities, buoys and shipping hulls that potentially complicate maritime navigation and marine recreational activities (Davies et al., Reference Davies, Stuart and de Villiers1989; Bezuidenhout & Robinson, Reference Bezuidenhout and Robinson2020).
Importantly, this species is not always an extensive reef builder in all introduced sites. For example, in South Africa, it only forms small aggregations in some localities (Davies et al., Reference Davies, Stuart and de Villiers1989; McQuaid & Griffiths, Reference McQuaid and Griffiths2014; Bezuidenhout & Robinson, Reference Bezuidenhout and Robinson2020), likely due to the low temperatures (<20°C) in winter (Miranda et al., Reference Miranda, Kupriyanova, Rishworth, Peer, Bornman, Bird and Perissinotto2016). Furthermore, F. enigmaticus is most successful in higher temperatures usually associated with low oxygen conditions in which it may have an advantage over native species that are less tolerant of such conditions (Jewett et al., Reference Jewett, Hines and Ruiz2005). In New Jersey F. enigmaticus overcame the low winter temperatures by settling in thermal effluent from a nuclear plant (Hoagland & Turner, Reference Hoagland and Turner1980). This is an important consideration for climate change conditions because this species could become more widespread in areas where previously environmental conditions were not suitable for tropical and subtropical species.
The impact of alien serpulid species that have the potential to form extensive reefs may also depend on the availability of artificial structures. For example, the impact of Ficopomatus uschakovi introduced in the Tropical Pacific (Mexico) is considered minimal, probably because of the absence of artificial hard substrates in the lagoon where it was introduced (Bastida-Zavala & García-Madrigal, Reference Bastida-Zavala and García-Madrigal2012). By contrast, Hydroides dianthus formed reefs over hard artificial substrata in an artificial coastal lake in China; here the serpulid reefs provided a habitat for the settlement and proliferation of the native jellyfish Aurelia coerulea in the lake (Dong et al., Reference Dong, Sun and Wang2018). The presence of serpulids over artificial substrates has been observed in structures of aquaculture facilities in the Mediterranean where Hydroides elegans and Hydroides dirampha were part of the community of hard substrata around a fish farm (Mangano et al., Reference Mangano, Ape and Mirto2019). In hard artificial substrates in the Mumbai harbour in India, the serpulid Protula tubularia was reported as a dominant alien species (Gaonkar et al., Reference Gaonkar, Sawant, Anil, Krishnamurthy and Harkantra2010).
The use of natural hard substrates by alien serpulids has also been documented in the Mediterranean, where H. elegans and H. dianthus build mass calcareous structures associating with beds of Mytilus galloprovincialis providing new microenvironments (Çinar et al., Reference Çinar, Kataǧan, Koçak, Öztürk, Ergen, Kocatas, Önen, Kirkim, Bakir, Kurt, Doǧan and Özcan2008). In other cases, aggregations of Hydroides operculata and ‘Spirobranchus kraussii’ (its taxonomic status is discussed below) have been observed both in natural and artificial hard substrates in the Mediterranean, where they cause changes in the benthic community structure and represent a potential additional impact for shipping activities (Çinar, Reference Çinar2006). Alien serpulids are also not limited to using hard substrates. In the English Channel Neodexiospira brasiliensis was reported as biofouling native eelgrass Zostera marina and the native algae Fucus serratus as well as the alien algae Sargassum muticum (Critchley et al., Reference Critchley, Farnham and Thorp1997).
Serpulids are not the only polychaetes that form reefs. Another important intertidal reef-building species is the spionid Boccardia proboscidea that clearly displays how context dependent environmental impacts can be. In its native range it occupies a wide ecological niche, burrowing into muddy and sandy sediments as well as into soft rock and crevices among encrusting algae (Hartman, Reference Hartman1940; Woodwick, Reference Woodwick1963; Gibson et al., Reference Gibson, Paterson, Taylor and Woolridge1999). But as an alien, this tube-dweller builds reefs in intertidal areas previously enriched by organic matter coming from sewage discharges in Mar del Plata (Argentina) (Jaubet et al., Reference Jaubet, Sánchez, Rivero, Garaffo, Vallarino and Elías2011). This species differs from F. enigmaticus as the reefs, that may be 1 to 5 m2 in diameter and up to 30 cm in height, are formed from sandy tubes and can take different forms that can evolve into a continuous platform, as is typical in impacted environments (Garaffo et al., Reference Garaffo, Jaubet, Sánchez, Rivero, Vallarino and Elías2012). However, unlike F. enigmaticus, these reefs cannot be seen as biodiversity hotspots, as the presence of this species demonstrates great environmental deterioration (Garaffo et al., Reference Garaffo, Jaubet, Sánchez, Rivero, Vallarino and Elías2012). Some of the negative impacts of B. proboscidea includes that its spread resulted in the eventual smothering of the native mussel Brachiodontes rodriguezii and a reduction in the diversity in the epilithic intertidal community in the sewage impacted sites in Mar del Plata (Jaubet et al., Reference Jaubet, Garaffo, Sánchez and Elías2013; Elías et al., Reference Elías, Jaubet, Llanos, Sanchez, Rivero, Garaffo and Sandrini-Neto2015).
The success of B. proboscidea is associated with its opportunistic and poecilogonous nature (r-strategy), which allows it to produce both planktotrophic and adelphophagic larvae (Simon & Sato-Okoshi, Reference Simon and Sato-Okoshi2015). Furthermore, they thrive under conditions of organic enrichment either from sources of sewage effluent (Jaubet et al., Reference Jaubet, Bottero, Hines, Elías and Garaffo2018) or from high accumulation of nutrients coming from abalone farms where B. proboscidea is a secondary boring species that has infested cultured abalone shells (Simon et al., Reference Simon, Ludford and Wynne2006). Due to these characteristics, this spionid has been classified as tolerant to moderate and high levels of organic contamination and could be used as an environmental indicator (Saracho Bottero et al., Reference Saracho Bottero, Jaubet, Llanos, Becherucci, Elías and Garaffo2020).
All this background is important for environmental managers to consider, as the establishment, progression and outcome of an invasion may be dependent on what a specific species' reaction is to a novel environment.
Another group of tube-building polychaetes that are widely investigated are the sabellids. These polychaetes can form dense three-dimensional colonies, allowing them to function as ecosystem engineers. But unlike the serpulids, their tubes are made of hardened secreted mucus and are usually covered with algae debris and shell fragments and the colonies occur in the subtidal (Arias et al., Reference Arias, Giangrande, Gambi and Anadón2013a, Reference Arias, Richter, Anadón and Glasby2013b; Douglas et al., Reference Douglas, Townsend, Tait, Greenfield, Inglis and Lohrer2020).
The filter-feeding S. spallanzanii (80–400 mm in length) is one of the largest species in the family Sabellidae with a leathery tube and spiral feeding fan that can reach 10–15 cm in diameter which markedly modifies local water currents and rates of sediment deposition (Hutchings, Reference Hutchings1999; O'Brien et al., Reference O'Brien, Ross and Keough2006). However, the magnitude of the impact is not clear-cut. Cohen et al. (Reference Cohen, Currie and McArthur2000) suggested that in Australia, S. spallanzanii established in high numbers in subtidal habitats that were most likely unoccupied by native species, while Ross et al. (Reference Ross, Keough, Longmore and Knott2007) suggested that the effects of the species on soft sediment assemblages could be negligible. However, experiments in situ showed that this sabellid strongly influences recruitment of other sessile taxa (e.g. barnacles, bryozoans and sponges) (Holloway & Keough, Reference Holloway and Keough2002a, Reference Holloway and Keough2002b) or the post-colonization process of other macrofauna (O'Brien et al., Reference O'Brien, Ross and Keough2006). In fact, most of the studies conducted in Australia and New Zealand showed that this species causes changes in the composition of macrofauna and nutrient cycling with regards to the process of denitrification and bacterial communities (Ross et al., Reference Ross, Longmore and Keough2013; Atalah et al., Reference Atalah, Floerl, Pochon, Townsend, Tait and Lohrer2019; Tait et al., Reference Tait, Lohrer, Townsend, Atalah, Floerl and Inglis2020). It has even been suggested that the presence of S. spallanzanii increased the local biodiversity, although this increase probably also included other alien species (Douglas et al., Reference Douglas, Townsend, Tait, Greenfield, Inglis and Lohrer2020). Thus S. spallanzanii induces the same cascade effects observed for F. enigmaticus, but in a different ecological niche.
Similar impacts have been observed in the Mediterranean with other alien sabellids. Branchiomma bairdi is particularly abundant in degraded areas such as harbours and marinas, where their tubes influence and modify the habitat (Arias et al., Reference Arias, Giangrande, Gambi and Anadón2013a, Reference Arias, Richter, Anadón and Glasby2013b). However, a positive aspect of this sabellid in the Mediterranean is its efficiency in removing bacteria which may counteract the effects of microbial pollution, thus playing a potential role for in situ bioremediation (Stabili et al., Reference Stabili, Licciano, Lezzi and Giangrande2014).
Tube dwellers have also been implicated in having a negative impact on economically important molluscs. For example, experiments conducted in situ in the Mediterranean suggest that the sabellid Branchiomma boholense dominate the use of substrates over the mussel M. galloprovincialis (Lezzi & Giangrande, Reference Lezzi and Giangrande2018). Also, aggregations of the North-west Atlantic bamboo maldanid Clymenella torquata, an intertidal tube-dwelling ecosystem engineer widely distributed in British Columbia (Canada) and established in Samish Bay (Washington), create a spongy porous substrate that has proved detrimental to local commercial oyster farms (who typically grow oysters on the bottom of mudflats), causing the oysters to sink into the sediment and suffocate (Mach et al., Reference Mach, Levings, McDonald and Chan2012).
As previously mentioned, impacts of shell borers in farmed molluscs are usually due to species of the Spionidae family that live in burrows within the shells of cultured molluscs, reducing the hosts’ shell integrity, growth, survivorship and market value (Spencer et al., Reference Spencer, Martinelli, King, Crim, Blake, Lopes and Wood2020). Which species become problematic depend on their ability to reach mollusc farms and flourish under different culture conditions, enabling some species to become pests (Simon & Sato-Okoshi, Reference Simon and Sato-Okoshi2015). Once established on farms, alien worms may spread even further when they escape from the farms and infest indigenous molluscs and disperse as larvae (Moreno et al., Reference Moreno, Neill and Rozbaczylo2006; Williams et al., Reference Williams, Matthee and Simon2016). This release of alien boring species from mollusc farms to the natural ecosystem may have negative impacts on the native fauna (Radashevsky & Olivares, Reference Radashevsky and Olivares2005). For example, in Australia it was found that the boring activity of the alien species B. proboscidea, Boccardia pseudonatrix and Polydora hoplura caused major damage in both cultivated and native molluscs especially when compared with the boring activity of native polydorid species in native mollusc species (Sato-Okoshi et al., Reference Sato-Okoshi, Okoshi and Shaw2008). Furthermore, the alien boring species Boccardia tricuspa and Polydora ricketsii coexisted with native boring species (Dipolyodra huelma and Dodecaceria opulens) on both cultivated and natural mollusc populations in Chile (Neill et al., Reference Neill, Rozbaczylo, Villaseñor-Parada, Guzmán-Rendón, Sampértegui and Hernández2020). Such alien species pose a great risk to commercial oyster farms. For example, in the Wadden Sea the alien Polydora websteri infested oyster reefs of the alien Pacific oysters Crassostrea (Magallana) gigas that are located close to commercial oyster farms, representing a potential economic problem to the oyster farms (Waser et al., Reference Waser, Lackschewitz, Knol, Reise, Wegner and Thieltges2020), following what occurred in the Pacific west coast of the USA, where P. websteri was introduced recently and has considerably impacted commercial oyster farms of C. gigas (Martinelli et al., Reference Martinelli, Lopes, Hauser, Jimenez-Hidalgo, King, Padilla-Gamiño, Rawson, Spencer, Williams and Wood2020).
The eradication of an alien boring polychaete species in aquaculture facilities is a complex process. The only documented case of successful eradication of an alien polychaete species is of the shell-boring sabellid Terebrasabella heterouncinata, introduced to the coasts of California as an epizoic contaminant on South African abalone imported in the 1980s (Culver & Kuris, Reference Culver and Kuris2000). This pest caused extensive shell deformities and greatly retarded body growth of abalone in mariculture farms in the introduced area (Leighton, Reference Leighton1998). The successful control of this species began with the correct taxonomic identification, conducted by Fitzhugh & Rouse (Reference Fitzhugh and Rouse1999) as at the moment of the infestation neither genus nor species had been described. To mitigate the impact of this species during 2002–2006 all the native gastropods (potential hosts) were removed from close to the aquaculture facilities to avoid the dispersal of T. heterouncinata. This, together with thermal and fresh water treatments in the mariculture farms to eliminate the pest on the abalone, meant that T. heterouncinata was no longer detected in subsequent monitoring in the area (Leighton, Reference Leighton1998; Culver & Kuris, Reference Culver and Kuris2000; Moore et al., Reference Moore, Juhasz, Robbins and Grosholz2007). Thus, the control and management of alien polychaete shell-boring species begins with a correct taxonomic identification and continues with quick actions before the alien species reach the stage of establishment and spread.
The impacts of alien spionids are not limited to reef-builders or shell-borers, but also includes infaunal species occupying soft-bottom sediments. In the Baltic Sea the alien M. viridis is not as conspicuous as the aforementioned species as it is part of the infauna where it is a burrowing deposit feeder, although it may also filter-feed (Dauer et al., Reference Dauer, Maybury and Ewing1981). The reason for the notoriety of this species was not its size (reach a length up to 10 cm), but its high abundance of 2600 to almost 20,000 individuals m−2 and the greater depth to which it burrows (20–40 cm) relative to native fauna (Essink & Kleef, Reference Essink and Kleef1988; Zmudziński, Reference Zmudziński1996). The bioturbation caused by the burrowing activity of M. viridis in the sediment could potentially affect redox conditions, modify diagenetic reaction pathways and change the microbial community structure (Kristensen et al., Reference Kristensen, Hansen, Delefosse, Banta and Quintana2011; Quintana et al., Reference Quintana, Hansen, Delefosse, Banta and Kristensen2011). Although some authors suggest that this species occupied an empty niche (Essink et al., Reference Essink, Eppinga and Dekker1998), a study conducted by Kotta & Ólafsson (Reference Kotta and Ólafsson2003) suggests that M. viridis could compete for food with the native amphipod Monoporeia affinis.
Although M. viridis is morphologically similar to its alien sibling species Marenzelleria arctia and Marenzelleria neglecta in the Baltic Sea, Renz & Forster (Reference Renz and Forster2013) observed in laboratory experiments that these three species have shown important ecological differences in their bioturbation of the sediment and therefore the authors did not recommend a functional grouping of these sibling species. This is once again an important indication that even in apparently closely related species there are important ecological differences.
Infaunal alien polychaetes have also been implicated in studies on marine pollution and benthic community composition. In the Mediterranean, alien polychaetes such as Desdemona ornata, F. enigmaticus, Polydora cornuta and Streblospio gynobranchiata have contributed up to almost 50% of the polychaete community in polluted areas (Çinar et al., Reference Çinar, Balkis, Albayrak, Dagli and Karhan2009). Similarly, changes in benthic community structure near polluted sources indicated the presence of alien polychaetes Glycinde bonhourei and Notomastus mossambicus (Çinar et al., Reference Çinar, Katagan, Öztürk, Dagli, Açik, Bitlis, Bakir and Dogan2012). Furthermore, in an integrative study that included an analysis of biodiversity and its relation with chemical and plastic pollution, alien polychaete species Kirkegaardia dorsobranchialis, Notomastus aberans, Pista unibranchia, Pseudonereis anomala and B. bairdi were found in polluted areas (D'Alessandro et al., Reference D'Alessandro, Esposito, Porporato, Berto, Renzi, Giacobbe, Scotti, Consoli, Valastro, Andaloro, Andaloro and Romeo2018). Contrastingly, on the coast of California the presence of the alien species Pseudopolydora paucibranchiata did not appear to have a negative impact on the benthic community but was rather associated with high diversity, probably due to the biogenic structures built by this species that enhances the abundance of other macrofauna (Ranasinghe et al., Reference Ranasinghe, Mikel, Velarde, Weisberg, Montagne, Cadien and Dalkey2005).
The 40 polychaete species reviewed here represent only about 13% of species globally reported as probably being alien (Çinar, Reference Çinar2013). Thus, a small proportion of known alien polychaetes have had their impacts investigated, but this is likely an underestimation. There is, for example, no doubt that impacts of alien species were investigated before the 1980s, but these studies and species would not have been included in this review if the species investigated were not identified as alien, or not identified to species level. This is especially relevant to shell-boring pests of mariculture. For example, the impact of an alien Polydora species on oysters in Australia was first reported in the late 19th century when Whitelegge (Reference Whitelegge1890) investigated oyster disease – the species was identified as Polydora ciliata, which was originally described on the south coast of England (Johnston, Reference Johnston1838). The identification as P. ciliata is doubtful, and Blake & Kudenov (Reference Blake and Kudenov1978) suggested that all records of P. ciliata in Australia are probably P. websteri, also an alien in Australia. Ogburn et al. (Reference Ogburn, White and Mcphee2007) proposed that a Polydora species (possibly the one investigated by Whitelegge (Reference Whitelegge1890)) brought to Australia on oysters imported from New Zealand, may have contributed to the disappearance of oyster reefs from estuaries in Eastern Australia. Impacts of more alien species have therefore probably been conducted before 1980, as reported here. By contrast, the taxonomy of many species purported to be alien are also in need of revision. For example, after thorough revision of the literature and specimens, Langeneck et al. (Reference Langeneck, Lezzi, Del Pasqua, Musco, Gambi, Castelli and Giangrande2020) found that of 86 polychaete species previously reported as alien along the Italian coast, only 25 (30%) could be confirmed as alien, while 3 were cryptogenic, 40 questionable and 18 were native or had been misidentified. Thus, estimates of alien polychaetes in many regions may have been exaggerated.
Impacts of species which are alien but erroneously investigated as indigenous (e.g. Rice et al., Reference Rice, Lindsay and Rawson2018), or not classified as alien (e.g. Schleyer, Reference Schleyer1991), would not have been reviewed here. For example, M. viridis was initially recorded as Marenzelleria wireni in the early 1980s during routine monitoring in the Wadden and Baltic Seas (Essink & Kleef, Reference Essink and Kleef1988; Zmudziński, Reference Zmudziński1996; Thomsen et al., Reference Thomsen, Wernberg, Silliman and Josefson2009) but a revision by specialists indicated that it actually was M. viridis (Essink & Kleef, Reference Essink and Kleef1988). Similarly, B. proboscidea was not always considered an alien in Mar del Plata, Argentina and was reported as Boccardia polybranchia in the early 2000s (e.g. Elías et al., Reference Elías, Rivero and Vallarino2003, Reference Elías, Rivero, Palacios and Vallarino2006). A revision conducted in 2009 by taxonomic specialists determined that the correct identification was B. proboscidea (Jaubet et al., Reference Jaubet, Sánchez, Rivero, Garaffo, Vallarino and Elías2011) so the previously published papers about the polychaetes in this area did not consider it as an alien. It is even possible that the Boccardia species identified in the earlier papers (Elias et al., Reference Elias, Vallarino and Bremee2000; Orensanz et al., Reference Orensanz, Schwindt, Pastorino, Bortolus, Casas, Darrigran, Elías, López Gappa, Obenat, Pascual, Penchaszadeh, Piriz, Scarabino, Spivak and Vallarino2002; Vallarino et al., Reference Vallarino, Rivero, Gravina and Elías2002; Adami et al., Reference Adami, Tablado and López Gappa2004; Martin & Bastida, Reference Martin and Bastida2008) were all of B. proboscidea.
With regards to the species labelled as CG, although F. enigmaticus is one of the most widespread alien polychaetes around the world, its true origin is still unclear (Dittmann et al., Reference Dittmann, Rolston, Benger and Kupriyanova2009) and recent molecular studies revealed that it is a species complex (Styan et al., Reference Styan, Mccluskey, Sun and Kupriyanova2017; Yee et al., Reference Yee, Mackie and Pernet2019). In the case of H. dianthus, a higher haplotype diversity in the Mediterranean seems to contradict the currently accepted native range of H. dianthus sensu stricto in the USA, while a molecular analysis is necessary to corroborate the status of H. operculata as alien in the Mediterranean because it is a complex of at least three cryptic species (Sun et al., Reference Sun, Al-Kandari, Kubal, Walmiki and Kupriyanova2017). For the sabellids B. bairdi and B. boholense, molecular and morphological evidence suggested important considerations in the identification of these species as alien in the Mediterranean (Del Pasqua et al., Reference Del Pasqua, Schulze, Tovar-Hernández, Keppel, Lezzi, Gambi and Giangrande2018).
The impact of ‘S. kraussii’ was investigated as an alien species in the Mediterranean Sea (Çinar, Reference Çinar2006). However, morphological and molecular analysis conducted by Simon et al. (Reference Simon, van Niekerk, Burghardt, Ten Hove and Kupriyanova2019) confirmed that this species is restricted to southern African coasts and belongs to a globally distributed complex of morphologically similar species. Similarly, the impact of P. paucibranchiata was reported on the Pacific coast of the USA (Ranasinghe et al., Reference Ranasinghe, Mikel, Velarde, Weisberg, Montagne, Cadien and Dalkey2005) and in the Mediterranean Sea (Dagli & Çinar, Reference Dagli and Çinar2008), but a recent taxonomic revision concluded that this species must be considered a complex of four pseudocryptic species (Radashevsky et al., Reference Radashevsky, Malyar, Pankova, Gambi, Giangrande, Keppel, Nygren, Al-Kandari and Carlton2020). In the case of P. websteri, this species was confirmed recently by molecular and morphological analyses as an alien in the Wadden Sea, west coast of the USA and South Africa (Martinelli et al., Reference Martinelli, Lopes, Hauser, Jimenez-Hidalgo, King, Padilla-Gamiño, Rawson, Spencer, Williams and Wood2020; Waser et al., Reference Waser, Lackschewitz, Knol, Reise, Wegner and Thieltges2020; Rodewald et al., Reference Rodewald, Snyman and Simon2021; Spencer et al., Reference Spencer, Martinelli, King, Crim, Blake, Lopes and Wood2020). However, the native range of this species is now being questioned. It was originally described from the east coast of the USA (Hartman in Loosanoff & Engle 1943), but recent genetic evidence suggests an Asian origin (Rice et al., Reference Rice, Lindsay and Rawson2018). However, there are reports of P. websteri in South America (Netto & Gallucci, Reference Netto and Gallucci2003; Breves-Ramos et al., Reference Breves-Ramos, Lavrado, Junqueira and da Silva2005; Sabry & Magalhães, Reference Sabry and Magalhães2005; Diez et al., Reference Diez, Radashevsky, Orensanz and Cremonte2011; Keppel et al., Reference Keppel, Keith, Ruiz and Carlton2019), Canada (Bergman et al., Reference Bergman, Elner and Risk1982; Bower et al., Reference Bower, Blackbourn, Meyer and Nishimura1992; Clements et al., Reference Clements, Bourque, McLaughlin, Stephenson and Comeau2017), Red Sea (Elnaby, Reference Elnaby2019), South Africa (Schleyer, Reference Schleyer1991), New Zealand (Handley, Reference Handley1995) and Australia (Nell, Reference Nell2001) that need to be confirmed by a molecular and morphological systematic review, as do reports of P. cf. websteri in some regions of South America (Oscar Díaz & Liñero-Arana, Reference Oscar Díaz and Liñero-Arana2009; Barros et al., Reference Barros, Gomes Santos, De Assis and de Souza2017). It is evident that the identification and distribution of P. websteri still needs a careful revision around the world. Finally, Allita succinea is reported from the Baltic Sea but its status as alien is uncertain (Thomsen et al., Reference Thomsen, Wernberg, Silliman and Josefson2009).
In summary, it is clear that taxonomic investigations are key to clarify species' status as indigenous, alien or cryptogenic (Hutchings & Lavesque, Reference Hutchings and Lavesque2020; Langeneck et al., Reference Langeneck, Lezzi, Del Pasqua, Musco, Gambi, Castelli and Giangrande2020; Malan et al., Reference Malan, Williams, Abe, Sato-Okoshi, Matthee and Simon2020), and will play a vital role in advancing the research on impacts of alien polychaete species.
Once the taxonomic status of an alien polychaete species is confirmed, the next challenge is the evaluation of its impact. It was clear that the scales and contexts of impact evaluations were heterogeneous across the studies considered here and this could introduce bias in the assignment of impact mechanisms. The classification proposed by Blackburn et al. (2014) is applicable at different levels of ecological complexity and different spatial and temporal scales. The impact mechanisms assigned in the present review were based on the best available evidence and are by no means definitive or complete. Impact categories are subject to change as more impact studies are undertaken and completed, especially in under-studied studied species. However, despite these limitations, the available data suggest that most species have a major to massive impact on the ecosystems they occupy. This indicates the importance of the study, prevention and management of polychaete alien species. Although, it may also indicate that species are only detected and studied once impacts have become obvious and massive.
The first strategy to detect and determine the impact of alien polychaete species is implementing a long series of marine ecosystem monitoring (Hoagland & Turner, Reference Hoagland and Turner1980; Nichols & Thompson, Reference Nichols and Thompson1985; Essink & Kleef, Reference Essink and Kleef1988). The selection of monitoring sites should prioritize entry points for introductions of alien species, such as ballast water discharge areas, docks, marinas and aquaculture sites with imported stocks, as well as nature conservation sites (Olenin & Minchin, Reference Olenin, Minchin, Wolanski and McLusky2011). Some monitoring programmes sample sediment (Nichols & Thompson, 1985) or use growth panels, made of wood or artificial substrates such as PVC, submerged in water and/or sediment to analyse the settlement times and cumulative growth of boring and fouling organisms (Hoagland & Turner, Reference Hoagland and Turner1980; Holloway & Keough, Reference Holloway and Keough2002a, Reference Holloway and Keough2002b; Mangano et al., Reference Mangano, Ape and Mirto2019). When alien species are accidentally introduced by aquaculture facilities the application of programmes like the one applied to the sabellid T. heterouncinata can lead to extirpation of well-established local pests (Culver & Kuris, Reference Culver and Kuris2000). Before the application of such programmes, evaluation using theoretical models such as the one conducted by Soliman & Inglis (Reference Soliman and Inglis2018) to predict the spread and economic impact of S. spallanzanii as a biofouler of aquaculture species, are useful to justify the level of biosecurity intervention. When an alien species such as F. enigmaticus is introduced in an estuarine system, a routine monitoring and strategic removal programme could limit its spread and negative impacts (Bezuidenhout & Robinson, Reference Bezuidenhout and Robinson2020). However, if an alien polychaete species is established in an open marine ecosystem, there is usually no way to extirpate or control the spread of populations as seen in the case of M. viridis in the Baltic Sea. Leppäkoski et al. (Reference Leppäkoski and Heidelberg2002) mentioned that in addition to the monitoring of alien species and studying their biology and ecology, no actions have been undertaken to address the problem in the Baltic Sea. Hence, the prevention of further introductions of alien species should be a priority for any marine biosecurity strategy.
Any national action programme aimed at preventing alien polychaete introductions needs to be supported by international collaboration and regulation, as the primary introduction of alien marine polychaete species have been via aquaculture and shipping activities (Jensen & Knudsen, Reference Jensen and Knudsen2005; Davidson et al., Reference Davidson, Zabin, Chang, Brown, Sytsma and Ruiz2010). For example, antifouling paints containing copper on commercial and recreational vessels help to prevent the introduction of alien species. However, the use of these paints is controversial as their accumulation in embayments could simultaneously affect the recruitment of indigenous species or facilitate the transport and establishment of copper-tolerant alien species into disturbed estuarine habitats (Dafforn et al., Reference Dafforn, Glasby and Johnston2008). For these reasons, an efficient control of the aquaculture industry and the development of new antifouling agents or techniques are key in preventing new introductions of alien species (Thomsen et al., Reference Thomsen, Wernberg, Silliman and Josefson2009). Finally the application of molecular barcoding and automatic image analysis could be helpful for early detection if followed by an immediate and more detailed taxonomic study of the unusual species (Olenin & Minchin, Reference Olenin, Minchin, Wolanski and McLusky2011).
Impacts of alien polychaete species are greatly under-studied and the research field needs to be developed. In the 150 studies included in our systematic review, some aspects of the impacts of 40 alien polychaete species were studied. It identified eight mechanisms of impacts which were mainly massive in magnitude for the alien polychaete species documented. The impact mechanisms (IMos) of alien polychaete species were strongly related to their biology and lifestyles; we found that the species that build conspicuous reefs and tubes mainly showed physical and structural impact on ecosystems and that shell-borers, mainly parasitism and infaunal species, showed mainly chemical, physical and structural impacts on ecosystems. We consider it a priority to produce correct taxonomic identifications using morphological and molecular tools to achieve reliable identifications to confidently determine the alien status of a species. Clearly, evaluating the impacts of an alien polychaete species, even a conspicuous one, is complex and subject to many variables. For this reason, the study of the impacts of alien polychaete species must be conducted in an interdisciplinary manner to integrate different ecological aspects of the species to find the best integrative adaptive solutions for the management of such alien species.
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315422000315.
The authors confirm that the data supporting the findings of this study are available within the article [and/or its supplementary materials].
A. A.-A. and H. v. R. would like to thank to Tammy Robinson-Smythe from Stellenbosch University for her orientation during the course ‘An introduction to Meta-analysis’. We would also like to thank Evangelina Castillo-Olguin for her help with generating the world-map graphs.
A.A.-A., and C. S. designed the study, A. A.-A. conducted the analysis and design of graphics, H. v. R. conducted part of the introduction and reviewed the grammar and references in all sections of the manuscript. All authors co-drafted the manuscript together. All authors read and approved the final version of the manuscript.
This systematic review was funded by National Research Council (NRF) of South Africa.
Conflict of interest
The authors declare that they have no conflict of interests.