Distribution and ecology of the recently introduced tanaidacean crustacean Sinelobus vanhaareni Bamber, 2014 in the northern Baltic Sea

The non-indigenous tanaidacean crustacean Sinelobus vanhaareni Bamber, 2014 was first found in northern Europe in 2006 and has since spread to the northern Baltic Sea. Here, we surveyed the distribution of the species in different habitats in southwestern Finland, focusing on vegetated macroalgal and seagrass habitats (i.e., Fucus vesiculosus beds and Zostera marina meadows). We also evaluated its potential impacts by synthesizing current knowledge on the traits and ecology of the species, and identified knowledge gaps. We found that S. vanhaareni is now present throughout most of the southwestern Finnish coast, in a number of vegetated and non-vegetated substrates down to 25 m depth. Furthermore, the presence of egg-brooding females in most areas also confirms that the population is self-sustaining. The species is especially abundant in shallow macroalgal belts and eelgrass meadows, which are critical habitats for biodiversity, ecosystem functioning, and ecosystem service provisioning, highlighting the need to understand the effects of S. vanhaareni in these important ecosystems. Its presence on boat hulls and in marinas and harbours suggests that recreational boating may be a major spread vector, while drifting macroalgal fragments may also contribute to regional spread. At this stage of invasion, we found high overlap in epifaunal community composition in sites where S. vanhaareni was present and sites where it was absent. Based on the functional traits of S. vanhaareni and closely related species, we infer that it is likely part of the detritus-based pathway in benthic food webs. However, additional sampling and experiments are necessary to determine the true extent of its distribution and to quantify trophic links (through stable isotope analysis, gut content analysis, and experimental trials) to fully understand its effects on communities and trophic networks in the northern Baltic Sea.


Introduction
The spread of non-indigenous species has become increasingly common in marine and estuarine ecosystems globally, mostly due to increased human activity and maritime transport throughout the 20 th century (Ruiz et al. 1997;Leppäkoski and Olenin 2001). The Baltic Sea is no exception, as the total number of introduced or cryptogenic (i.e. of unknown origin) species is currently estimated at 140, of which approximately 78 have established permanent populations (Ojaveer et al. 2017). Furthermore, invasion rates in the region have accelerated since the 1950s as maritime transport and shipping activities have grown (Leppäkoski and Olenin 2000;Leppäkoski et al. 2002). During the latest assessment period (2011)(2012)(2013)(2014)(2015)(2016) of core indicators of the ecological status of the Baltic Sea, twelve new species were recorded (HELCOM 2018), including the tanaidacean Sinelobus vanhaareni (Bamber 2014; Figure 1).
This tanaidacean was first noted in Europe in 2006, in the Netherlands and Belgium (van Haaren and Soors 2009). At the time, it was identified as Sinelobus stanfordi Richardson, 1901, a widely distributed cosmopolitan species, which was believed to be the sole member of the genus Sinelobus. In 2009-2010, it was subsequently observed in several locations in the German North Sea (Brzana et al. 2019), Dutch Wadden Sea (Gittenberger et al. 2010) and Estonian Baltic Sea (G. Reisalu pers. comm.). Multiple additional observations of the species have since been made throughout the North and Baltic Seas (Estonia, France, Finland, Germany, Latvia, Lithuania, Netherlands, Poland;AquaNIS 2015), and it has established dense breeding populations in some areas such as in the Gulf of Gdanśk (Brzana et al. 2019). Re-examination of the genus has since revealed multiple species within the genus Sinelobus (e.g. Bamber 2008Bamber , 2014Rishworth et al. 2018), and the species present in northern Europe was named Sinelobus vanhaareni (Bamber 2014). Both its origin and initial mode of introduction to northern Europe remain unknown. However, it was never sighted in the Baltic Sea prior to 2010 despite intensive coastal ecological research in the area, and it is officially listed as a non-indigenous species in the Baltic Sea by HELCOM (HELCOM 2018) and by countries in which it has been sighted (e.g. by the Finnish Advisory Board for Invasive Alien Species, appointed by the Ministry of Agriculture and Forestry; www.vieraslajit.fi).
Relatively little is known about S. vanhaareni, or its congener S. stanfordi. The genus Sinelobus belongs to the family Tanaididae in the order Tanaidacea (Sieg 1980;Bamber 2014;Anderson 2016). These small tubedwelling malacostracan crustaceans are characterised by a prominent pair of clawed chelipeds and the presence of a marsupium (brood pouch) in which the larvae develop and emerge without a dispersive larval phase (Johnson and Attramadal 1982;Błażewicz-Paszkowycz et al. 2012). Tanaidaceans are found in a wide range of habitats, including but not limited to stromatolites (Rishworth et al. 2019), wood (Błażewicz-Paszkowycz et al. 2015, shallow coral reefs (García-Madrigal et al. 2005), deep-sea corals (Jakiel et al. 2015), plant roots (Hendrickx and Ibarra 2008;Slivak et al. 2013), vegetated and bare soft sediments (Ferreira et al. 2015;Kassuga et al. 2017), turf algae (Rishworth et al. 2018), and natural and artificial hard substrates (Bamber 2012;Brzana et al. 2019;Rumbold et al. 2015). We assume that the basic morphological and reproductive characteristics of tanaidaceans are present in S. vanhaareni, but species-specific data on its life history, habitat preference, and diet are lacking, making it difficult to determine its ecological role in the northern Baltic Sea.
Sinelobus vanhaareni was found in Finnish waters for the first time in 2016, in the western Gulf of Finland (Finnish Biodiversity Information Facility, Supplementary material Table S1, Figure 2). It has been present since at least 2013 in Muuga Harbour, near Tallinn (G. Reisalu pers. comm.), on the Estonian coast of the Gulf of Finland. This may be its point of introduction to Finland, due to heavy recreational boating and commercial shipping between Estonia and Finland in this area. Since 2016, several individuals have occasionally been reported in the Gulf of Finland, Archipelago Sea, and Bothnian Sea during water and benthos monitoring programmes (Räisänen 2018;Holmberg et al. 2020;Räisänen and Koivunen 2020;Vahtera et al. 2020), but no dedicated research or monitoring for the species exists. However, following numerous sightings in 2019-2020, there is an increased interest in understanding the potential impacts of this rapidly spreading non-indigenous species. Our aims in this study were to (1) describe the current distribution and density of S. vanhaareni in different habitats along the Finnish coast, (2) determine whether invertebrate communities in vegetated habitats (Fucus vesiculosus Linnaeus, 1753 and  Table S1) and where it was absent from samples taken in the course of this study (see "Field sampling" section in methods). Different colours indicate the studied habitat, a filled circle or triangle indicates presence of S. vanhaareni and a cross indicates absence of S. vanhaareni. The red star indicates the location of the first reported sighting in Finland.
Zostera marina Linnaeus, 1753) differ in the presence and absence of S. vanhaareni, and (3) synthesize current knowledge and identify knowledge gaps in the traits and ecology of the species to assess potential impacts on communities and trophic networks.

Materials and methods
The data in this study were collected using a number of different sampling methods across the southern and southwestern Finnish coast and Åland Islands (Table 1, Figure 2). These samples were collected as part of several ongoing research projects studying the biodiversity of coastal habitats. We supplemented this data with sightings reported on the online portals of the Finnish Advisory Board for Invasive Alien Species (www.vieraslajit.fi) and the Finnish Biodiversity Information Facility (www.laji.fi), published reports of benthos and water monitoring from municipalities, and as-of-yet unpublished data from ongoing monitoring efforts of boats, marinas, and harbours by the environmental NGO "Keep the Archipelago Tidy" Association and the Finnish Environment Institute SYKE.

Field sampling
In 2018 and 2019, we sampled infauna at 5 sites in the Åland Islands (2 eastern and 3 southern) with an Ekman bottom grab (3 replicates, 0.0289 m 2 , sieved at 0.5 mm) from unvegetated soft sediments (2-5 m depth). The sampling was done twice each year, in June and in August.
In July 2020, we sampled epifauna associated with filamentous algae (mostly composed of Cladophora glomerata and Ulva intestinalis) on hard substrates at 9 sites in the Archipelago Sea. The algae were collected randomly by hand at 0.5 m depth at each site. We measured the dry weight of the algae in each sample.
In July 2020 we also sampled epifauna associated with bladderwrack F. vesiculosus on hard substrate in the central Gulf of Finland (8 sites), Archipelago Sea (from inner to outer archipelago, altogether 24 sites), northeastern and western Åland Islands (10 and 7 sites, respectively), and southern Bothnian Sea (6 sites). The samples were taken from 0.5-1 m depth using mesh bags (mesh size 0.5 mm) and sieved through a 0.5 mm sieve. 6 replicates in total were taken at each study site, 3 from the sheltered and 3 from the exposed sides of small rocky islands. We measured F. vesiculosus wet weight of each sample and estimated the F. vesiculosus dry weight using dry weight:wet weight ratio (based on a ratio measured for 10 random F. vesiculosus thalli).
In August-September 2020, we sampled epifauna (9-10 replicates, Ø 20 cm mesh bags, mesh size 0.5 mm) and infauna (5 replicates, Ø 10.5 cm corer, sieved at 0.5 mm) from 4 eelgrass (Z. marina) meadows on soft substrate in the Gulf of Finland, the Archipelago Sea, and the Åland Islands. For the epifauna samples, we also measured Z. marina aboveground (i.e. shoot) dry weight of each sample.
For all field sampling methods, we calculated the mean density of S. vanhaareni in each site and reported densities (Table S1) relative to sampling area (individuals m -2 ) and to vegetation dry weight (individuals g dw -1 ) for epifaunal samples. Salinity throughout the study areas is relatively stable (ca. 5-6), and, while sampling of different habitats was conducted at different time points, sampling within a habitat type was always conducted during the same season. Thus, the effect of salinity, temperature and successional state of the community should have had minor effects on the community composition within each substrate type.
Community analyses were conducted in PRIMER-E v6 (Clarke and Gorley 2006) on the abundance of each taxon in each sample separately for F. vesiculosus and Z. marina habitats. The data were square root transformed, and the resemblance matrices were calculated based on Bray-Curtis similarity. Differences between communities with and without S. vanhaareni were analyzed with ANOSIM. Global-R in ANOSIM indicates how similar communities are on a scale from 0 to 1, with 1 indicating complete dissimilarity and values < 0.2 indicating a high degree of similarity and overlap (Clarke and Gorley 2006). The differences in community composition were visualized in multidimensional scaling (MDS) plots. Due to the technical limitation of multivariate analyses, the nested structure of the data was ignored, and all samples from each site were considered independently in the analyses (but taken into account when interpreting the data).

Functional traits
To assess the potential impacts of S. vanhaareni on ecosystem functioning and trophic networks, we undertook a literature review to determine functional traits and information on trophic links. As we found little literature on this species, we also collected trait data on the closely related S. stanfordi and the southern Baltic species Heterotanais oerstedii Krøyer, 1842. We selected traits related to life history, habitat, reproduction, dispersal, and trophic relationships (Table 2), based on previous studies of infaunal functional traits in the Baltic Sea (e.g. Törnroos and Bonsdorff 2012). Life history, reproduction and dispersal traits provide information on the potential spread of the species, while traits linked to habitat give insight about which habitats are likely affected and the potential physical effects of the species on habitats (e.g. bioturbation, nutrient cycling, etc.). Lastly, trophic traits provide insight on the potential impacts of the species on trophic networks.

Distribution and abundance
Sinelobus vanhaareni was present throughout the southwestern Finnish coast in 2018-2020, including the Gulf of Finland, Archipelago Sea, southern Bothnian Sea, and Åland Islands, with the highest densities (up to 1500 individuals m -2 ) observed in epifaunal samples from vegetated habitats including Z. marina and F. vesiculosus (Table S1, Figure 2). In 2020, the population of S. vanhaareni in these vegetated habitats was concentrated in the eastern parts of the inner and middle Archipelago Sea and in the southern Bothnian Sea (Figure 2). Individuals were also found in several other shallow hard-and soft-substrate habitats, including mud, sand, and among filamentous algae growing on rocks (Table S1, Figure 2). These included adult individuals of both sexes, including egg-brooding females in all areas. Additional sightings were also noted from deeper (10-25 m) benthic habitats (mud and clay) in five coastal municipalities (Helsinki, Naantali, Porvoo, Rauma, Turku; Räisänen 2018; Holmberg et al. 2020;Räisänen and Koivunen 2020;Vahtera et al. 2020;Turkki 2021) and from small boats, hard surfaces, and fouling plates in six marinas and harbours (Hanko, Kasnäs, Raisio, Ruoholahti, Satava, Vuosaari;Outinen et al. 2021).

Community analyses
Epifaunal community composition in F. vesiculosus differed significantly between communities with and without S. vanhaareni, but the differences between these communities were negligible due to high overlap (ANOSIM Global R = 0.175, p < 0.001), which was also visible on the MDS plot ( Figure 3A). The epifaunal community composition in Z. marina also differed significantly between communities with and without S. vanhaareni, but contrary to F. vesiculosus, this difference was notable (ANOSIM Global R = 0.513, p < 0.001) and clearly visible on the MDS plot ( Figure 3B). However, this effect was likely driven by differences in overall community structure between the sampled sites (ANOSIM Global R = 0.926, p < 0.001), and not driven solely by the presence of S. vanhaarenii. As the majority of samples (9 of 11) that contained S. vanhaareni were from the same site, additional data would be needed to properly assess if there are differences in community structure due to S. vanhaareni presence at a much larger geographical scale.

Functional traits
We found that basic morphological and reproductive traits of tanaidaceans were well documented, and this study reported, for the first time, the distribution and abundance of S. vanhaareni across different habitats and depths in the northern Baltic Sea (Table 2). However, the literature review revealed that several important gaps remain, particularly relating to life span, reproductive frequency, and trophic interactions.

Discussion
Since being first reported in Finland in 2016 near Inkoo in the western Gulf of Finland (Finnish Biodiversity Information Facility), the nonindigenous tanaidacean Sinelobus vanhaareni is now present throughout the southern and southwestern Finnish coast, from the central Gulf of Finland and throughout the Archipelago Sea up to the Bothnian Sea and Åland Islands. Egg-brooding females were observed in all sampled areas in July-September 2020 ( Figure S1), indicating that the species is reproducing in Finnish waters and that the population is likely self-sustaining. However, we found no small juvenile individuals. Either the eggs hatch later in the season, or the newly-hatched juveniles were too small (< 0.5 mm) to be included in our samples. Year-round sampling using a smaller mesh size would be needed to fully understand the life cycle and phenology. As the species has little dispersal capacity due to its small size and lack of pelagic larval phase, human-mediated vectors have probably contributed to spread of this magnitude. Shipping, in particular ballast water and hull transfer, is an important vector for non-indigenous marine species (Ojaveer et al. 2017) and has been noted as a vector for another tanaidacean Tanais dulongii (Rumbold et al. 2015). Brzana et al. (2019) suggested that spread of S. vanhaareni throughout the southern Baltic Sea has likely occurred through fouling on ship hulls. This is also likely to be the case in Finland, though we suggest that recreational boating, which is very popular in the area, may also be a major spread vector, as multiple individuals have been found on small boat hulls and hard surfaces in harbours and marinas (J. Vuolamo pers. comm.). The high abundance of S. vanhaareni on the brown alga Fucus vesiculosus suggests that drifting fragments of F. vesiculosus (Rothäusler et al. 2015) could also contribute to the spread of the species along the coast. Tanaidaceans are widely distributed and have been recorded from a number of different habitats, substrates, and depths in different parts of the world (García-Madrigal et al. 2005;Hendrickx and Ibarra 2008;Bamber 2012;Slivak et al. 2013;Błażewicz-Paszkowycz et al. 2015;Ferreira et al. 2015;Kassuga et al. 2017;Jakiel et al. 2015;Rumbold et al. 2015;Rishworth et al. 2018Rishworth et al. , 2019. In this study, we found that S. vanhaareni also occupied a broad range of infaunal and epifaunal habitats, including mud, clay, sand, filamentous algae, Z. marina shoots, and F. vesiculosus thalli. In Z. marina meadows, S. vanhaareni seems to be more abundant as epifauna on vegetation than as infauna in the sediment. This suggests that the species benefits from the habitat complexity offered by aboveground vegetation which provides refuge, food, and shelter from disturbances (e.g. Pihl 1986;Boström and Bonsdorff 2000). Its presence across multiple habitat types, substrates, and depths, including artificial substrates in human environments and anoxic and oil-polluted sediments (e.g. Holmberg et al. 2020), also suggests a high degree of persistence and tolerance to environmental conditions. As communities with and without S. vanhaareni were highly overlapping, we found no evidence (using a space-for-time approach) that it has significantly altered the macrofaunal community composition associated with F. vesiculosus, at least at this stage of spread. However, we were unable to assess this in other habitats such as Z. marina, as it was only abundant in one site. Similarly, shifts in meiofaunal community composition could not be tested here, as the sampling methodology did not target small meiofaunal species below 0.5 mm. The effects of S. vanhaareni in different habitats definitely merit further attention, as its high abundance in some sites suggests potential for altering ecosystem functioning and/or trophic networks as it continues to spread. Due to the low native biodiversity of the Baltic Sea, non-indigenous species have previously introduced novel traits and trophic links, leading to shifts in ecosystem functioning, community structure, and trophic interactions (Kotta et al. 2006;Packalén et al. 2008;Aarnio et al. 2015;Jormalainen et al. 2016). The magnitude of a nonindigenous species' impacts is highly context-dependent (Thomsen et al. 2011), depending on the species in question, the recipient community, and environmental conditions in the recipient habitat. Determining the traits and trophic links of a new non-indigenous species is therefore the first step in evaluating its potential impacts.
However, as with the majority of non-indigenous species in the Baltic Sea (Ojaveer et al. 2021), studies quantifying or even documenting the effects of S. vanhaareni on Baltic food webs are lacking. To our current knowledge, there are no records of S. vanhaareni trophic interactions or any studies on its role in the food web using e.g. gut contents analysis (visual or molecular approaches) or stable isotope analysis in any areas. However, inference based on its functional traits, phylogeny, and distribution in different habitats, as well as documented trophic interactions of related species in other parts of the world, suggests that S. vanhaareni in the Baltic Sea is: (i) Likely part of the detritus-based pathway in benthic food webs in shallow coastal areas (and possibly to depths of down to 25 m) and plays a role in meiofaunal community structure due to its small size. (ii) Feeding mainly on detritus and associated microorganisms (e.g. algal particles, nematodes; Bückle Ramírez 1965; Heiman et al. 2008;Rishworth et al. 2018). Although S. vanhaareni increases the taxonomic diversity of the community, as there are no other tanaidacean species in the northern Baltic Sea, it is likely contributing to the functional redundancy of small epifaunal and infaunal invertebrate detritivorous consumers, such as amphipods and polychaetes, rather than increasing functional richness. It could thus potentially have an indirect positive effect on macrophyte growth by feeding on epiphytic microalgae and detritus (Hughes et al. 2004). (iii) Likely a prey/food item for small benthic feeding fish and crustacean species, such as gobies, juvenile flounder, sticklebacks, perch, shrimp, etc., which feed on other small crustaceans such as amphipods (see Nordström et al. 2015 and references therein). Beyond trophic interactions, S. vanhaareni could also potentially affect ecosystem functioning, sediment dynamics and small-scale biogeochemistry in soft substrates, through its tube-building and bioturbation activities in a similar way to infaunal amphipods (Rhoads and Boyer 1982).
Determining the actual distribution of this species, along with confirming and quantifying the trophic links above (through stable isotope analysis, gut content analysis, and experimental trials) are key to addressing knowledge gaps and understanding its effects on Baltic Sea communities and trophic networks. Public observations of conspicuous invasive species in Finland are usually readily reported to online portals, providing a reliable source of information on their distribution and spreading rates. However, as S. vanhaareni is small and inconspicuous, there are very few public observations. Therefore a dedicated monitoring programme would be necessary to determine the true distribution of this species and assess its impacts. Monitoring of harbours, ship hulls, and ballast water for non-indigenous species in the Baltic Sea is underway in the ongoing COMPLETE project (https://balticcomplete.com/), but based on the data collected here, we suggest that a monitoring programme targeting this species should also include a wide variety of natural habitats and artificial substrates along a large depth gradient (at least 0-25 m).

Conclusions
Though small and inconspicuous, S. vanhaareni has quickly become more frequently observed since its initial recorded sighting in Finnish waters, with its spread possibly aided by recreational boating and drifting algal fragments. The species now occurs in a variety of habitats and environments, from unvegetated sediments down to 25 m depth, to seagrass and algal habitats in shallower waters. Sinelobus vanhaareni also seems persistent and tolerant to a wide range of environmental conditions, as it has been recorded in environments with clear human impacts such as boat hulls, marinas, and anoxic and oil-polluted sediments. It is likely part of the detritus-based pathway in the food web, but several functional traits and trophic connections are still unverified. Thus, its potential effects on coastal ecosystems are uncertain, opening up many avenues for further research into the ecological role of this species in the northern Baltic Sea.

Funding declaration
Sampling of Zostera marina habitats was funded by the Maj and Tor Nessling Foundation (grant 201900244, KG). Sampling of Fucus vesiculosus habitats was carried out within the VELMU programme, funded by the Finnish Ministry of the Environment and within the ÅlandSeaMap project, funded by the Baltic Sea Conservation Foundation and the European Maritime and Fisheries Fund through the Government of Åland (HR). The latter also partially funded the sampling of infauna in Åland (HH). Sampling of filamentous algae was funded by the MAAMERI project through the Finnish Ministry of the Environment (TS), and benthos sampling in the Archipelago Sea and Bothnian Sea was funded by Societas pro Fauna et Flora Fennica (JW). MCN and SS-L were supported by the Åbo Akademi University Foundation, and HH by the Åbo Akademi University doctoral network in Functional Marine Biodiversity (FunMarBio).