Distribution and abundance of Talitridae in the southern Baltic Sea – twelve years after the first record of Platorchestia platensis (Krøyer, 1845) in 2005
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Introduction
The family Talitridae currently consists of 80 genera and 512 species occurring all over the world (Horton et al. 2018). They include beach fleas and sandhoppers, which are semiterrestrial bimodal breathers (Spicer & Taylor 1987) – they either bury themselves in moist sand or live among stranded decaying algae (Backlund 1945; Zettler & Zettler 2017). Cryptic species are discovered and described every year, suggesting that the taxonomy of Talitridae is at an early stage of development (e.g. Wildish 2017). So far, four species of Talitridae have been recorded in the southern Baltic Sea: two indigenous species – Talitrus saltator (Montagu, 1808) and Deshayesorchestia deshayesii (Audouin, 1826) and two presumably non-indigenous species – Cryptorchestia garbinii (Ruffo, Tarocco & Latella, 2014) and Platorchestia platensis (Krøyer, 1845) (Ojaveer et al. 2017). In addition to these four species, two other species of Talitridae, Orchestia gammarellus (Pallas, 1766) and Britorchestia brito (Stebbing, 1891), occur in the catchment area of the Baltic Sea and adjacent territories (Zettler & Zettler 2017).
The indigenous talitrids, T. saltator and D. deshayesii, inhabit supralittoral sandy beaches in the southern and western Baltic Sea. During the day, they hide in burrows close to a high water mark to avoid desiccation stress (Williams 1983) and emerge at night to feed on nearby stranded macrophytes (Bulheim & Scholl 1986; Fallaci et al. 1999; Ayari-Akkari et al. 2014). T. saltator and D. deshayesii often co-occur (Drzycimski & Nawodzińska 1965). D. deshayesii was first recorded in the study area by Drzycimski and Nawodzińska (1965), who found it only on the Hel Peninsula (Puck Bay).
It has been suggested that the populations of T. saltator and D. deshayesii have declined in the Baltic Sea area (HELCOM 2013a,b). According to the HELCOM Red List, T. saltator can be classified into the “data deficient” category and D. deshayesii – into the “vulnerable” category. In Poland, T. saltator is legally protected
1 Regulation of the Minister of the Environment of 16 of December 2016 on the protection of animal species (Dz. U. 2016, item 2183)
, whereas D. deshayesii is not protected by law. Studies on the distribution and abundance of T. saltator and D. deshayesii (as Talorchestia deshayesii) on the southern Baltic Sea coast were carried out in 1961–1963 (Drzycimski & Nawodzińska 1965). After that, research on T. saltator was carried out in 1997 (Węsławski et al. 2000a).
C. garbinii is presumably a non-indigenous species in the Baltic Sea (Ojaveer et al. 2017). According to recent molecular studies, C. garbinii is closely related to other species from the genus Cryptorchestia inhabiting the eastern Mediterranean regions. The evolution of C. garbinii could have been a pattern of recent east-to-west dispersal, with a more recent northward expansion (Davolos et al. 2004; 2018). The information about the arrival and invasion vector is extremely limited. C. garbinii was recently described by Ruffo, Tarocco & Latella (2014) as a new species, previously identified as C. cavimana. In the Baltic Sea, C. garbinii was first recorded (as O. litorea) at the end of the 19th century (Selgio 1899) in the southern part only (former West Prussia). P. platensis is a cosmopolitan species distributed both in the temperate and tropical regions (Behbehani & Croker 1982). It was originally described from Montevideo in Uruguay in 1845 by Krøyer (1845). However, its place of origin is unclear due to the fact that this site was close to the international port of Montevideo (La Fontaine 1902). According to the latest studies, P. platensis is a non-indigenous species in Europe, genetically related to the populations across the Atlantic (Hupało & Grabowski 2018). In the Baltic Sea, P. platensis was first found in Denmark in the northern part of Øresund in 1860 (Dahl 1946), then in the 1930s and 1940s it appeared to be common on both sides of Øresund and the Swedish coast of Kattegat. It expanded its distribution along the German and Swedish coast of the Baltic Sea (Backlund 1945; Dahl 1946; Urbański 1948; Karlbrink 1969; Zettler 1999; Persson 2001). P. platensis was first reported in Poland from the Hel Peninsula in Puck Bay in 2005 (Spicer & Janas 2006). Elsewhere, P. platensis can coexist with indigenous species, sometimes successfully outcompeting them (e.g. Dahl 1946; Karlbrink 1969; Persson 2001). So far, no coexistence of P. platensis with other Talitridae in the southern part of the Baltic Sea has been observed.
Although talitrids play an important role in the food web and they serve as a link between marine and terrestrial ecosystems, they have received little attention from marine or terrestrial biologists. T. saltator is likely to be the most important of the macrofaunal consumers of the stranded macrophyte detritus (Jędrzejczak 2002; Adin & Riera 2003). The importance of talitrids, especially T. saltator, in the food web was emphasized by the study of their biochemical composition (El Gtari et al. 2013).
The objective of this research was to answer the following questions: (1) what is the Talitridae species composition, distribution and abundance in the southern Baltic Sea, (2) has non-indigenous P. platensis extended its range of occurrence since the introduction, (3) do non-indigenous species co-occur with indigenous species and (4) in what types of habitats do individual Talitridae species occur?
Materials and methods
Forty three sampling sites were established in the supralittoral zone, roughly every 10 km along 500 km of the entire Polish Baltic Sea coast (Węsławski et al. 2000a) (Fig. 1, Appendix). The field work was conducted from 12 August to 16 September 2017. Five replicates were collected at each sampling site within a distance of 1 m from each other, parallel to the coastline, at the boundary between wet and dry sand. Each sampling location was categorized by the habitat type according to our observations and the presence or absence of stranded flora. Three habitat-type categories were established: bare sand – 16 study sites, sand with plants – 21 sites, boulders with plants – 6 sites. At each sampling site, talitrids were collected through the core sampling, using a hand corer (diameter 10 cm, depth 20 cm) as described in the HELCOM guidelines (HELCOM Combine 2014). Each sample was sieved through a 1 mm mesh. The material left on the sieve was transferred to plastic containers and preserved. All amphipods were preserved in 96% ethanol, except T. saltator, which was identified in situ, counted, photographed and released. The identification of T. saltator was based on its morphological features: the shape (broader toward the head) and the pattern on the dorsal side, i.e. a longitudinal dark line along the pereion and pleosome with two or several perpendicular short symmetric stripes or shades as in Photo 1. in Spicer & Janas (2006). The identification of other Talitridae was completed in the laboratory following the identification keys for Talitridae (Lincoln 1979; Spicer & Janas 2006; Zettler & Zettler 2017). The collected wrack was preserved in 96% ethanol, then washed with tap water in the laboratory, dried to wet mass using a salad spinner and then further dried on blotting paper and weighed on a scale (accuracy of 0.0001 g). Talitridae density was expressed as a number of individuals per m2 (ind. m−2). The relationship between the biomass of wrack and amphipod density was determined by Spearman’s rank correlation coefficient test. The difference between the densities in different habitat types was tested using the Mann-Whitney U-test for T. saltator and P. platensis. Differences between densities of four Talitridae species on sandy habitat was tested by the Kruskal-Wallis rank sum test and pairwise comparison was tested using Dunn’s-test for multiple comparisons of independent samples with Bonferroni’s p-adjustment method. Prior to the statistical analysis, the normality of the data was tested (Shapiro-Wilk test p < 0.05). All statistical analyses were conducted using R 3.4.4. and Dell Statistica 13.1. The cartographic visualizations were carried out using Esri ArcGIS Pro 2.0.1.
Figure 1
Talitridae distribution and density in the southern Baltic Sea
Results
Four Talitridae species were found at the sampling sites: T. saltator, D. deshayesii, C. garbinii and P. platensis. O. gammarellus was not recorded. The Talitridae occurred at 20 out of 43 sampling sites, which accounts for 47% of the surveyed area. T. saltator was recorded at 14 sampling sites (33% of the surveyed area), D. deshayesii – at three sampling sites (7%), P. platensis – at seven sampling sites (16%) and C. garbinii – at two sampling sites (5%). T. saltator occurred both at the coast of the open sea and in the Gulf of Gdańsk. The three other species, D. deshayesii, P. platensis and C. garbinii, were found only around the Gulf of Gdańsk (Fig. 1).
The highest mean densities of T. saltator (over 600 ind. m−2) were recorded at three sampling sites (21, 27 and 30; Appendix). At nine sampling sites, the density of T. saltator ranged from 50 to 250 ind. m−2 and at only one sampling site (41) it was less than 50 ind. m−2 (25 ind. m−2) (Fig. 1). The average density of T. saltator at places of its occurrence reached over 200 ind. m−2.
The highest average densities of P. platensis (over 5000 ind. m−2) were determined at sites 26 and 35 (Appendix). At only two sampling sites the density was less than 50 ind. m−2 (sites 27, 37) (Fig. 1). The average density of P. platensis was about 2000 ind. m−2.
The highest average density of D. deshayesii was recorded at site 27 (280 ind. m−2). At one sampling site (30), the average density was 152 ind. m−2 and at one site (35) it was 25 ind. m−2 (Fig. 1, Appendix).
C. garbinii was recorded at two sites. At one site (37), the average density was 102 ind. m−2. By the Dead Vistula River (site 38), the average density reached 1299 ind. m−2 (Fig. 1, Appendix).
At two sampling sites, non-indigenous P. platensis was found together with indigenous species: T. saltator and D. deshayesii (Fig. 2). At one sampling site (30), two indigenous species co-occurred (T. saltator and D. deshayesii) and at one site (37) – non-indigenous species co-occurred (P. platensis and C. garbinii) (Fig. 2).
Figure 2
Talitridae species composition in the Gulf of Gdańsk, southern Baltic Sea
Most of the southern Baltic Sea coast is homogeneous, represented mainly by open sandy beaches. More diverse habitats occur within the Gulf of Gdańsk, where, in addition to sandy beaches, boulder areas occur more often (Appendix). At the open sea coast, the common component of wrack was Fucus vesiculosus L. and Zostera marina L., whereas Z. marina dominated in the Gulf of Gdańsk, both on sandy beaches and boulders.
D. deshayesii occupied only sandy habitats with stranded wrack (Fig. 3). T. saltator was found exclusively on sandy beaches, both with and without stranded wrack. The density of T. saltator was significantly higher in sandy habitats with stranded wrack than on bare sand (Mann-Whitney U-test, p < 0.05). The frequency of T. saltator was higher in the habitat with stranded wrack (Fig. 4).
Figure 3
Density of Talitridae in different habitats (with a break in the ordinate axis)
Figure 4
Frequency of Talitridae in different habitats
P. platensis was the only species that occurred on a habitat with boulders. In addition to areas with boulders, it also occurred in the same habitats as indigenous species, i.e. sandy beaches. The density of P. platensis differed significantly between habitats, with the higher density in the boulder area (Mann-Whitney U-test, p<0.05) (Fig. 3). The frequency of P. platensis at sites with boulders reached 67% (Fig. 4).
The density of four studied Talitridae species on sandy beaches with stranded wrack was significantly different (Kruskal-Wallis test, p <0.001). The density of T. saltator was significantly higher than all other species (post hoc Dunn’s-test, p <0.05) (Fig. 3).
The density of P. platensis was positively correlated with wrack biomass (Spearman’s test, rs = 0.619, p < 0.000000001). The positive correlation between the density of T. saltator and wrack biomass was also significant (Spearman’s test, rs=0.468, p <0.02).
Discussion
Declining sandhopper populations
T. saltator is still a common inhabitant of the exposed sandy beaches along the southern Baltic Sea coast, but it has disappeared from a number of previously occupied localities (Fig. 5). In the study from the 1960s, T. saltator occurred along the entire southern Baltic Sea coast, with the highest densities on the open sea coast (Drzycimski & Nawodzińska 1965).
Figure 5
Distribution and density of T. saltator in 1963 (Drzycimski & Nawodzińska 1965), in 1997 (Węsławski et al. 2000a) and in 2017 (this study)
Densities exceeding 250 ind. m−2 were recorded at 45% of the sampling sites. D. deshayesii was found only on the Hel Peninsula, where at one site the species co-occurred with T. saltator. In the 1990s, a significant decline in the density of T. saltator, as well as a decrease in its distribution area were observed (Węsławski et al. 2000a). In the 1990s, T. saltator was found in 40% of the surveyed area and its density did not exceed 250 ind. m−2 and was lower than 50 ind. m−2 in 76% of the sampling sites (Fig. 5). However, it should be noted that the methods of sampling were not identical during the conducted studies. Węsławski and others (2000a) sampled one square meter within the most populated areas, but Drzycimski and Nawodzińska (1965) collected the talitrids from an undefined area, at a depth of up to 25–30 cm. Neither samples were sieved.
Twenty years after the last research in 1997, an increase in the density of T. saltator was recorded, the average density of T. saltator in areas of its occurrence reached over 200 ind. m−2. The density of T. saltator was below 50 ind. m−2 at only 7% of the sampling sites, yet the abundance from the 1960s has not been reached. However, T. saltator was found in areas where it was previously not recorded, mainly in the Słowinski National Park. Nonetheless, T. saltator distribution has decreased in the study area. It was found in 33% of the surveyed area, while in 1997 the species inhabited 40% of the area. This may be related to tourism and mechanical beach cleaning, known to denude the coastal macrofauna (Dugan et al. 2003; Fanini et al. 2005). Considering the positive relationship between the density of T. saltator and wrack biomass, the wrack removal could affect the distribution of T. saltator. In addition to beach cleaning and other tourism-related activities, pollution and changes in trophic conditions, climatic changes such as storm frequency, severity of winters and sea level rise could also contribute to the reduction of the T. saltator distribution area (Węsławski et al. 2000a). T. saltator, once abundant in the southwestern part of the Gulf of Gdańsk (Drzycimski & Nawodzińska 1965), is no longer recorded in this area (Węsławski et al. 2000a). On the other hand, we observe that P. platensis is now present in the area.
The significant decrease in the abundance of T. saltator in 1997 could be related to the disappearance of seaweed meadows and decline of macroalgae species in the coastal waters of the southern Baltic during the pollution crisis in the 1970s and 1980s (Węsławski 2000a). Recently, a natural recovery of Z. marina meadows has been observed after a dramatic decline in the last century (Dąbrowska et al. 2016; Jankowska et al. 2018) and this may positively affect an increase in the T. saltator abundance. However, T. saltator has faced new challenges, like the potential invasion of the new talitrid, P. platensis.
Expansion by P. platensis
The first report on the colonization of the Baltic Sea by P. platensis came from the Scandinavian region (Dahl 1946) and we can currently presumably observe an ongoing secondary dispersal in the Baltic Sea (Persson 2001). P. platensis was first observed in Poland by Spicer & Janas (2006) in May 2005. At that time, it was recorded in only one area on the Hel Peninsula – in Kuznica (sampling site 26). Since then, P. platensis has apparently been gradually spreading around Puck Bay. In 2006, a survey by students (Kotwicki et al. 2009) recorded P. platensis at two sites, Kuznica and nearby Jurata (corresponding to our sampling sites 26, 27). In 2012, P. platensis was found at the end of the Hel Peninsula (site 29) (U. Janas, unpublished observations). By 2013, P. platensis spread to the other side of Puck Bay where it was recorded at sampling site 35, while the following year it reached sites 31 and 33. Our current data show a significant spread of P. platensis on the southern Baltic coast. P. platensis was recorded at seven sampling sites. It has reached Gdynia and Gdańsk (36, 37) and expanded its territory beyond the area of Puck Bay.
P. platensis occurred only around the Gulf of Gdańsk, where it was most likely introduced by synanthropic transport, taking under consideration the distance from the nearest German population and its absence along the open sea coast. The secondary dispersal in the Gulf of Gdańsk could involve passive transport by currents. P. platensis, as a beach flea living in beach-cast wrack, is more exposed to a swash risk and is likely to be passively transported by currents (Fanini & Lowry 2014). Fanini & Lowry (2014) tested the survival behavior of talitrids when swashed away and subjected to passive transportation. Talitrids were able to survive in seawater, to swim precisely and quickly head toward an object and then cling on it.
Our research confirms that P. platensis can be observed in a variety of habitats, like wrack beds, sandy shores, boulders and driftwood (Rasmussen 1973; Persson 2001; Lacey 2009), which is different from most beach fleas and sandhoppers. This could enhance the possible invasive character of P. platensis in the southern Baltic Sea. Since P. platensis occurs on rocky shores with stranded wrack, it is more likely to be dispersed via drifting wrack than T. saltator, which exclusively inhabits sandy beaches above the high-tide level, buried under the sand surface, which is reflected in the genetic structure of the populations of these species in the Mediterranean area (De Matthaeis et al. 2000).
P. platensis occurred mainly in areas with anthropogenic changes (six out of seven studied sites). It was initially discovered on boulders used for coastal reinforcement (sampling site 26). It has then spread to other nearby artificial substrates and has reached areas unchanged by human activity, where indigenous species occur. It can therefore be suggested that the anthropogenic environment favors non-indigenous P. platensis and supports its further spreading.
The density of P. platensis was positively correlated with wrack biomass. Such a strong correlation is presumably related to higher accumulation of wrack on artificial boulders. Thus, the removal of wrack from sandy beaches due to tourism-related mechanical beach cleaning affects mainly the distribution of T. saltator and not necessarily P. platensis, due to its habitat (i.e. boulders). The relationship with wrack biomass has been studied for another non-indigenous talitrid in the Baltic Sea – C. garbinii (Herkül et al. 2006). As with P. platensis, the occurrence of C. garbinii was positively correlated with wrack biomass.
Interactions between different talitrid species
Considering the coexistence of P. platensis with all other Talitridae species, it seems necessary to undertake further research on the ecology of Talitridae and the potential interactions between species on the southern Baltic Sea coast. The competition between P. platensis and other species, such as O. gammarellus, has been demonstrated for Swedish populations (Dahl 1946; Karlbrink 1969; Persson 2001). P. platensis outcompetes other species at lower salinities (Persson 2001) and up to 30% water loss (Morritt& Spicer 1998). Furthermore, P. platensis is a more active jumper than O. gammarellus, so it may be better at evading predators (Karlbrink 1969). P. platensis has presumably a longer reproductive period than T. saltator, which may account for the competitive superiority of this non-indigenous species (Dahl 1946; Węsławski et al. 2000b).
D. deshayesii
According to Drzycimski and Nawodzińska (1965), D. deshayesii occurred only on the Hel Peninsula from the side of Puck Bay, but its density remained unknown. In our research, D. deshayesii was found on both sides of Puck Bay, both at the Hel Peninsula and near Gdynia (sampling site 35), thus its area of distribution has increased. This study confirms that it is one of the rarest talitrids species in the Baltic Sea (Zettler & Zettler 2017).
C. garbinii
There are no previous studies on the abundance of C. garbinii or its distribution along the southern Baltic Sea coast, but it is likely that the area of its distribution has expanded. We observed that apart from previous sites (Żmudziński 1990; Konopacka et al. 2009), the species also occurred in Sobieszewo (sampling site 38), in a closed protected artificial dune established after creating the international Deepwater Container Terminal in Gdańsk. The dune was created using sand from a nearby beach. The presence of C. garbinii in this new area could be an effect of secondary dispersal from the Dead Vistula River or, given the proximity of the international harbor, this could be a new anthropogenic introduction. The population genetics research, like the one performed by Hupało and Grabowski (2018) on P. platensis, seems to be necessary to tackle the history of the introduction, because otherwise it will not be certain whether C. garbinii is non-indigenous species or not. C. garbinii is commonly found in damp habitats, beneath stones and decaying vegetation, close to fresh or brackish water (Spicer & Janas 2006; Konopacka et al. 2009). In the Gulf of Gdańsk, C. garbinii coexisted only with P. platensis.
Conclusions
Over the last five decades, changes in both indigenous and non-indigenous Talitridae species have occurred. The density of T. saltator has increased, but the area of its occurrence has decreased during the last two decades. The area of D. deshayesii occurrence has increased since the 1960s. T. saltator occurred along the cost of the open sea as well as in the Gulf of Gdańsk, while D. deshayesii, C. garbinii and P. platensis occurred only in the Gulf of Gdańsk. The non-indigenous species P. platensis has extended its range of occurrence and can coexist with both indigenous and non-indigenous species. P. platensis has successfully colonized the Gulf of Gdańsk and it has been observed in a variety of habitats, unlike other species of Talitridae. Nevertheless, little is known about the ecological role of talitrids and it seems necessary to undertake further research on their ecology and the potential interspecific interactions in the southern Baltic Sea.
