Macroinvertebrate communities on various microhabitats of a saline coal mine settling pond

Anthropogenic water bodies that are located in urban and industrial areas can be very important for aquatic fauna and flora, especially in areas where there are no natural water bodies (Gee et al. 1997; Gledhill et al. 2008;Vermonden et al. 2009;Chester & Robson 2013; Hassall 2014; Hill et al. 2016; Martínez-Abraín & Jiménez 2016; Rewicz et al. 2016; Hill et al. 2017). These anthropogenic habitats may be particularly important for rare and threatened species. For example, Lewin & Smoliński (2006) reported the presence of the rare gastropod species Anisus vorticulus (Troschel) and Valvata naticina Menke in clay pit ponds; the former is Near Threatened according to the European Red List of Non-marine Molluscs (Cuttelod et al. 2011) and the Red List of Threatened Animals in Poland (Głowaciński & Nowacki 2004), and the latter is Critically Endangered in Poland (Głowaciński & Nowacki 2004). Pakulnicka (2008) found a rare species of water beetles, Ochthebius hungaricus Endrödy-Younga, in a gravel pit pond, and Nowak et al. (2007) noted rare and threatened pondweed communities that had been formed by species from the genus Potamogeton (L.).

Some anthropogenic water bodies are associated with various technological processes including coal, brown coal, nickel, salt or sand mines (Echols et al. 2009; Jaruchiewicz 2014; Luek & Rasmussen 2017). The activity of mines is connected, among others, with the formation of settling ponds. These water bodies are used for temporary retention of saline mine waters before they are discharged into rivers, and therefore their waters are, among others, contaminated with salt (Echols et al. 2009).

It should be emphasized that until recently research on macroinvertebrate communities in settling ponds has rarely been undertaken. The research focused on the effects of drainage from surface coal mining operations on zoobenthos and indicated that settling ponds may create favorable conditions for various taxa of macroinvertebrates (Canton & Ward 1981). However, research on the saline settling ponds that are associated with underground coal mining has never been undertaken.

Anthropogenic salinization is one of the most important factors responsible for biological changes in aquatic biota (Bäthe & Coring 2011; Kang & King 2012; Arle & Wagner 2013), thus it is particularly important in the case of coal mine settling ponds whose waters are often very saline. It should be emphasized that saline inland water bodies can be unique habitats. Only a few submerged aquatic plants can grow and reproduce in conditions of high salinity. Among the submerged macrophytes, Ruppia (L.) has the highest tolerance to salinity (Triest & Sierens 2009). A preliminary study carried out in saline coal mine settling ponds in southern Poland resulted in the discovery of a Ruppia maritima (L.) locality in one of them. To the best of our knowledge, this is currently the only inland site of this species in Poland. R. maritima occurs both in the coastal zone of the seas and estuaries (Verhoeven 1979) as well as in freshwater environments (Lazar & Dawes 1991).

To date, research on invertebrates that inhabit widgeongrass beds has been carried out in estuaries (e.g. Fredette et al. 1990; Heck et al. 1995; Keats & Osher 2007; Henninger et al. 2009; Barnes & Ellwood 2012), lagoons (e.g. Por 1971; Casagranda et al. 2006), coastal habitats (e.g. Montague & Ley 1993; Boström & Bonsdorff 2000; Leopardas et al. 2014; Bartolini-Rosales et al. 2016) and various inland saline habitats such as streams (Velasco et al. 2006), ponds (Verhoeven 1978, 1980; Guerrini et al. 1998) and lakes (Brock & Shiel 1983; Wollheim & Lovvorn 1995; 1996; Herbst et al. 2013), while such research has never been undertaken in saline coal mine settling ponds.

The objective of the study was to verify whether various microhabitats affect the abundance and composition of macroinvertebrates in a saline settling pond. To test this, the research was carried out on microhabitats that occur in a settling pond such as R. maritima, Phragmites australis (Cav.) Trin. ex Steud and sediments with no macrophytes.

Because there are no data on the fauna of anthropogenic saline ponds, it is impossible to compare our results. It should be emphasized that the studies to date have focused primarily on the influence of water salinity on benthic invertebrates in rivers and streams. These studies have indicated that increased salinization results in the elimination of freshwater taxa and the replacement of sensitive species by eurytopic species and species that are resistant to high salt concentrations, including invasive non-native species (e.g. Braukmann & Böhme 2011; Petruck & Stöffler 2011; Arle & Wagner 2013; Cañedo-Argüelles et al. 2014).

Our studies have shown that the euryhaline amphipod Gammarus tigrinus, which is an alien species in Polish waters, dominated in all the microhabitats. It is possible that the species migrated into the studied settling pond from the Bierawka River and the Oder River where it was previously observed (Grabowski et al. 2009). Its great abundance in the investigated pond confirms the finding that anthropogenic salinization may cause the colonization and establishment of non-native species (Piscart et al. 2005; 2011). The high salinity tolerance (up to 25 PSU) and the high reproductive potential of G. tigrinus compared to other gammarids enables the species to colonize the most saline habitats in Europe (Bousfield 1969; Piscart et al. 2005; 2006; Grabowski et al. 2009; Braukmann & Böhme 2011; Petruck & Stöffler 2011). It often dominates the fauna of salt-polluted rivers, for example it reached 98.4% of the total number of all taxa in the Werra River (Braukmann & Böhme 2011). The colonization success of G. tigrinus in saline habitats may also be supported by the lack of native species that are excluded by salinity stress (Piscart et al. 2005). As a result, alien species often become the dominant groups in non-native regions (Alonso & Castro-Díez 2008; Ba et al. 2010; Bäthe & Coring 2011). However, Petruck & Stöffler (2011) indicated that G. tigrinus can inhabit environments with both the highest and the lowest chloride concentrations. The authors suggested that the correlation between its occurrence and water salinity preferences may not be very strong.

In addition to G. tigrinus, we also found the high salt-tolerant oligochaete species Paranais litoralis (O. F. Müller). It has been described as a cosmopolitan inhabitant of brackish waters and waters that receive saline pollution (van Haaren et al. 2017). Previously, it was reported only from the Polish coastal waters and the Baltic Sea (Marszewska et al. 2017). Our finding is the first record of this species in an inland habitat. P. litoralis might have been introduced into the settling pond by waterfowl and other migratory birds, which are a likely vector for the long-distance dispersal of oligochaetes (Milbrink & Timm 2001).

In the studied settling pond, we also observed the non-native gastropod species Potamopyrgus antipodarum (Gray), insect larvae from the genus Enallagma Charpentier (Odonata, Coenagrionidae) as well as the families Ceratopogonidae, Chironomidae (Diptera) and Corixidae (Heteroptera) that are considered halotolerant (Verhoeven 1980; Hammer et al. 1990; Williams & Williams 1998; Keats & Osher 2007). We also found other widely distributed damselfly species such as Ischnura elegans (Vander Linden) and Orthetrum albistylum (Selys), which have a high tolerance to salinity (Sato & Riddiford 2008). Our study highlights the importance of saline coal mine settling ponds as habitats for halotolerant invertebrates.

The results of our study are consistent with the findings of Hutchinson (1937), who stated that salt-tolerant species of the family Corixidae were much more abundant on widgeongrass beds compared to other aquatic macrophytes. We observed that their abundance was the highest in the first month of the study (June) and decreased by the end of the survey (Fig. 4). The reverse trend was determined for G. tigrinus (Fig. 3). Savage (1981) showed that due to the shortage of vegetable organic matter in sediments, G. tigrinus becomes carnivorous and may eat the nymphs of Corixidae. Furthermore, it may eliminate Corixidae by using the same food resources. It is possible that this phenomenon also occurs in the studied coal mine settling pond. The study by Wollheim & Lovvorn (1995, 1996) also showed much higher predator biomass than primary consumer biomass in a mesosaline lake (Lake Hutton, Wyoming, USA).

An unexpected result of our study was the relatively low seasonal variability of the macroinvertebrate richness on all the habitats. Similar results were observed by Wenner & Beatty (1988), Heck et al. (1995) and Boström & Bonsdorff (2000). The lack of taxa associated with a particular habitat suggests that the type of substrate is not a major determinant in the diversity of benthic assemblages and that these taxa showed no specific habitat preferences. One reason may be the mobility of the species (dominant taxa are good swimmers) and the degree of their aggregation (Wilson & Koutsagiannopolou 2014).

The results of our research on the macroinvertebrate biomass are consistent with the study by Kornijow et al. (1990), who noted that the biomass of zoobenthos was lower on P. australis than on other studied macrophytes. The biomass and abundance of the macrofauna associated with R. maritima in the investigated settling pond were low compared to previous studies of widgeongrass meadows (Verhoeven 1980; Boström & Bonsdorff 2000; Keats & Osher 2007). However, much lower fauna abundance on R. maritima was estimated in a New England estuary by Heck et al. (1995). Murkin et al. (1992), who found lower abundance of invertebrates in submerged rather than emergent vegetation, suggested that this could be caused by stressful dissolved oxygen levels and fish predation as well as the fact that emergent plants produce more organic matter. In our study, the total dissolved oxygen was high (never lower than 10.2 mg O₂ dm^-3) and no aquatic vertebrate predators were found. Thus, the oxygen levels and predation had little effect on the abundance and biomass of macroinvertebrates. Similar results were reported by Wollheim & Lovvorn (1996) in saline lakes in the USA. They also indicated that macrophytes supported the greatest total biomass of invertebrates compared to unvegetated sediments and open water. Our results showed both the highest abundance and biomass on the widgeongrass beds compared to the two other microhabitats. This may be caused by the fact that vegetated habitats create heterogeneity and represent more valuable food resources such as epiphytic algae (Fredette et al. 1990; Guerrini et al. 1998). This indicates that widgeongrass meadows can be convenient habitats for fauna, not only in coastal waters but also in saline inland waters such as settling ponds.

Because there are no data on the fauna of saline coal mine settling ponds, it is important that the future research will focus on the biodiversity of macroinvertebrates, the rate of colonization by alien species and the relationships between taxa and habitat conditions.