Benthic foraminifera have rarely been reported from saline springs in Germany. To fill this gap, we investigated live (Rose Bengal stained) and dead benthic foraminifera from saline ponds, springs, and meadows in central Germany. For foraminiferal investigations, we collected surface samples along transects with changes in vegetation at Sülldorf in Saxony-Anhalt, in Artern and close to Auleben, Luisenhall, and Esperstedt in Thuringia. We found live and dead foraminifera at all investigated saline locations. We observed seven different agglutinated species that commonly inhabit coastal salt marshes (Trochamminita irregularis, Trochamminita salsa, Entzia macrescens, Miliammina fusca, Siphotrochammina lobata, Haplophragmoides manilaensis, and Haplophragmoides wilberti), one agglutinated species, Entzia sp., which has not been described to date, and one calcareous species, Gordiospira arctica, which has earlier been described from shallow-water settings at high northern latitudes. We hypothesize that foraminifera have been repeatedly transported to the inland saline habitats in central Germany by migratory birds on their routes from northern and southern Europe probably since the early Holocene. Future genetic investigations of the species in central Germany and comparisons with sequenced specimens from other localities will provide a better understanding of their provenance and phylogenetic position.

Benthic foraminifera are a diverse group of protists in fully marine environments but also occur in low diversity in intertidal environments such as salt marshes and mangroves. Although they are mainly restricted to marine and coastal settings, typical shallow-water foraminifera have been found in salt lakes in Egypt (e.g., Almogi-Labin et al., 1995; Abu-Zied et al., 2007), Canada (e.g., Boudreau et al., 2001), USA (Patterson, 1987), and southern Australia (Cann & De Deckker, 1981). They also have been reported from saline springs in Middle Asia (Brodsky, 1928; Mikhalevich, 1976) and from mineral springs in central Asia (Okuneva & Takhteev, 2007). In addition, fossil inland foraminifera were documented in sediments from the Aral Sea, central Asian and west Siberian lakes (e.g., Riedel et al., 2011; Burr et al., 2019), northern Saudi Arabia (Pint et al., 2017), and dune sands in India (Rao et al., 1989). Likewise, intertidal salt marsh foraminifera have been reported from inland salt ponds and meadows. For example, Entzia macrescens was found in Recent and late Holocene terrestrial salt-marsh sediments near Turda and Sic in Romania (von Daday, 1883, 1884; Filipescu & Kaminski, 2011; Telespan et al., 2017; Jakab et al., 2018; László et al., 2022). The species was also reported together with Annectina viriosa from Lake Winnipegios in Manitoba (Canada; Patterson et al., 1997). It was further observed together with Miliammina fusca in small lakes and ponds in Barbados, West Indies (Roe & Patterson, 2006), and as Trochammina sp. in saline lakes in Australia (Cann & De Deckker, 1981). Intertidal and shallow-water foraminifera have also been reported from Salt Lake, a neighborhood of Honolulu, on the island of O’ahu, Hawaii (Resig, 1974).

Intertidal benthic foraminifera also inhabit inland brackish ecosystems in northern and central Germany (Fig. 1A). Species attributed to the genera Elphidium and Ammonia were recorded in Holocene sediments from Salziger and Süsser See in Saxony-Anhalt (Wennrich et al., 2007), whilst empty tests of Haplophragmoides canariensis (= Haplophragmoides wilberti according to Resig (1974)) have been reported from salt ponds and springs close to Erfurt, Alperstedt, Stotternheim, and Siebleben (Thuringia) by Bartenstein (1939). Living (Rose Bengal stained) and dead Jadammina polystoma (= Entzia macrescens) have been found at Seckerrift and Barnstorf (Lower Saxony) by Haake (1982). Dead specimens of Entzia tetrastomella (= E. macrescens) were recovered by Rieth (1958) at Artern (Thuringia). Likewise, Kahl (1928) observed Entzia tetrastomella in salt ponds close to Bad Oldesloe (Schleswig Holstein).

These early observations from terrestrial saline springs and ponds suggest that only monospecific assemblages can thrive in these terrestrial environments. Since these observations were deemed exotic and foraminiferal investigations largely focused on marine environments, no further investigations were attempted and, hence, it remained unclear whether foraminifera were still present in saline springs, ditches, and ponds at recent times. The aim of this study consequently is to explore which benthic foraminiferal species prevail in surface sediments of terrestrial saline water bodies in central Germany, whether they still live there, and whether differences between the faunas or assemblages at the individual saline sites are recognizable. To accomplish these goals, we resampled locations of previous foraminiferal observations and other saline ponds and meadows in Saxony-Anhalt and Thuringia in central Germany.

The investigated salt ecosystems in Saxony-Anhalt, comprising Sülldorf, Osterweddingen, and Dodendorf, are situated south of Magdeburg and along the river Sülze (Fig. 1B). Common halophytes were Bolboschoenus maritimus, Suaeda maritima, Salicornia europaea, Glaux maritima, Aster tripolium, Puccinella sp., and Elymus spp. Water physico-chemical parameters were measured in situ in the saline spring and the brackish lake at Sülldorf in October 2022 (Fig. 2). The salinity was very high with 46.6 and 67.2 practical salinity units (PSU) at temperatures of 14.9 and 15.9°C; pH was 7.6 and 6.8; and oxygen content was 3.42 and 1.98 mg/l in the brackish lake and at the saline spring, respectively (Table 1). At Osterweddingen and Dodendorf, water measurements were made in the wetland meadows in October 2022. Salinity was low with 5.2 PSU at a temperature of 15.3°C at Osterweddingen, but higher at Dodendorf with 18.4 PSU at a temperature of 18.1°C; pH was comparable with 7.3 and 7.2, and oxygen content was 13.40 and 2.31 mg/l at Dodendorf and Osterweddingen, respectively (Table 1). More detailed information on the water chemistry and biology of the river Sülze can be found in the data portal of the Gewässerkundliche Landesdienst Sachsen-Anhalt (https://gld.lhw-sachsen-anhalt.de/?permalink=1vyMHn79).

The saline habitats investigated in Thuringia are situated in (1) northern Thuringia, south of the Kyffhäuser mountains close to Auleben, Esperstedt and at Artern (Fig. 1C), and (2) in central Thuringia, north of Erfurt and close to the small village Luisenhall (Fig. 1D). The vegetation observed at Auleben included Phragmites australis, Argentina anserina, Artiplex intracontintalis, Distichlis spicata, Euphorbia cyparissias, Lavatera thuringiaca, and Festuca rubra. Water chemistry was measured directly in the salt spring (Fig. 2). The salinity was low (5.9 PSU) at a temperature of 15.6°C. The pH was 7.1, and oxygen content was 2.35 mg/l (Table 1).

Close to Esperstedt, Spartina europaea was observed in a saline ditch, and abundant Phragmites australis, Chenopodium rubrum, and Festuca rubra were observed on the adjacent salt meadow. The saline water in the ditch (Fig. 2) had a salinity of 17.7 PSU at a temperature of 17.2°C, pH of 8.4, and a very high oxygen content of 19.65 mg/l (Table 1). The high oxygen content might be the result of an algal bloom observed in the ditch (Fig. 2).

At Artern, Spartina europaea, Halimione pedunculata, Artemisia maritima, Oenanthe fistulosa, Festuca rubra, and Triglochim maritimum were identified. Water measurements were made in the saline pond and in the nearby ditch (Fig. 2). Salinity was 33.4 and 20.3 PSU at temperatures of 16.6 and 14.4°C, pH was 8.2 and 7.3, and oxygen content was 8.84 and 10.94 mg/l, respectively.

Close to Luisenhall, the vegetation was dominated by Phragmites australis and Althaea officinalis. For more detailed information see Sparmberg et al. (2005). Water measurements were made in a pond on the farmland near the Luisenhall 2 transect and in a ditch with saline water where the Luisenhall 4 transect was sampled (Fig. 2). Salinity was low with 3.0 and 1.3 PSU at 14.5 and 11.3°C; pH was comparable with 7.0 and 7.3, and oxygen content was low with 4.20 and 3.83 mg/l, respectively (Table 1). Water measurements close to the Luisenhall 1 transect (Fig. 2), made in 2021, had higher salinities of ∼13 PSU (own unpublished data). Sparmberg et al. (2005) reported salinities of up to 40 PSU of the dried surface soil close to the salt pond near our Luisenhall 1 transect.

We investigated the halophytes and took a total of 19 surface samples along four vegetational transects at Sülldorf (Saxony-Anhalt) in July 2022, and we re-sampled two transects in October 2022 (9 samples). The vegetational transects at Sülldorf were sampled close to the Sülze river (Sud A1), close to an artificial branch (bypass) of Sülze river (Sud B1), close to a saline spring (Sud C1; Sud C2; Fig. 2) and close to Sülldorf brackish lake (Sud D1, Sud D2; Fig. 2). We took single surface samples from salt meadows at Dodendorf (Dod 1) and Osterweddingen (Ost 1) in Saxony-Anhalt in October 2022 (Figs. 1, 2).

The surface samples from Thuringia were taken on October 2022. At Auleben, we took a total of 12 samples along four vegetational transects (transects Au 1 to Au 4) at different distances to a saline spring and perpendicular to a saltwater ditch (Fig. 2). At Esperstedt, we took a total of seven samples from two transects. One transect was sampled in a saltwater ditch (Esp 1) and the other on a salt meadow (transect Esp 2; Fig. 2). At Artern, we took a total of 15 samples from three vegetational transects (Art 1 to Art 3) around an unvegetated pond (Fig. 2). At Luisenhall, we took a total of 16 samples from four vegetational transects, including saltwater ponds in a cultivated farmland (Luis 2 and 3) and one transect from an abandoned farmland (Luis 1; Fig. 2). Short transects, Luis 2 and 4, were sampled perpendicular to saltwater ditches.

We investigated surface samples taken along transect Sud C1, sampled in July 2022 at Sülldorf in Saxony-Anhalt; along transects Art 1, Au 1, and Esp 1, sampled in October 2022 at Artern, and close to Auleben and Esperstedt, situated in northern Thuringia; and along transect Luis 1, sampled close to Luisenhall in central Thuringia in October 2022 (Figs. 1, 2). We further screened all surface samples taken along the Sülldorf transects (Sud A1, Sud B1, and Sud D1) from July 2022, and one surface sample each from the other transects at Luisenhall (Luis 2 to Luis 4) and Esperstedt (Esp 2), and the single samples from Dodendorf (Dod 1) and Osterweddingen (Ost 1) for their foraminiferal content (Fig. 2). We did not screen samples from the other transects from Artern and Auleben because they are close to each other, had similar sampling schemes, and showed a similar vegetational succession.

All foraminiferal samples were taken from the uppermost centimeter of the surface sediment with a spoon. The volumes ranged from 22 to 50 cm3. They were preserved and stained with a solution of 2 g Rose Bengal per 1l g ethanol (95%, technical quality) on the day of sampling (Walton, 1952; Schönfeld et al., 2012), buffered with CaCO3 powder, and stored for at least four weeks before they were processed. All selected samples were washed through 500- and 63-µm sieves, and the 63–500-µm fraction was investigated. Some samples were very rich in foraminifera and thus had to be split in aliquots by using a wet-splitter after Scott & Hermelin (1993) to obtain a manageable sample size. Only bright and completely stained specimens (except of the last chamber) were considered as living at the time of sampling. Rose Bengal stained and dead specimens (empty tests) were counted separately. Taxonomic identification mainly followed the illustrations in Hawkes et al. (2010), Wright et al. (2011), Milker et al. (2015a), and Müller-Navarra et al. (2017) as well as online resources (WoRMS, 2022; Fig. 3, Appendix 1). Juvenile specimens of species and genera affiliated with the Trochamminidae family that could not be identified on species level were counted as “juvenile trochamminids”. One species was left in open nomenclature. Photographs of the observed species were made with the Hitachi TM 4000 tabletop scanning electron microscope (Fig. 3). Other, single or redundant surface samples were screened for their foraminiferal content. Thereafter, all investigated samples were stored in ethanol, buffered, and kept for later investigations.

We measured pH, conductivity, oxygen, and temperature of the water of saline springs, saltwater ditches, saline ponds, or lakes in the vicinity of the sampled transects in October 2022 (Table 1). The parameters were directly measured in the water with a handheld multimeter (Hach HQ2200). Additional to the samples taken for foraminiferal studies, samples for soil water conductivity and pH measurements were taken along all transects. The sediment samples were oven-dried at 38°C until they were completely dried and prepared according to DIN ISO 10390. In detail, 10 g of oven-dried soil was placed in 25 ml of demineralized water and shaken with a horizontal shaker for one hour and then rested another hour. The supernatant water was measured with a WTW Multi 340i handheld multimeter. One sample could not be measured because there was no water available after preparation, and some other samples had only a small volume of supernatant water so that some conductivity measurements might be too low (marked in Appendix 2). All conductivity measurements were converted into salinity using an online calculator (salinometry.com/ctd-salinity-calculator/).

Soil Water Chemistry and Benthic Foraminiferal Distribution Along the Transects

Sülldorf Transect (Saxony-Anhalt)

The soil water salinity along transect Sud C1 from Sülldorf (Saxony-Anhalt) ranged from 26.8 PSU in the sediment in the saline spring, to between 7.5 and 11.9 PSU in the soil at the other stations. The pH decreases from 7.5 to 7.3 with increasing distance from the saline spring (Fig. 4; Appendix 2).

We found between 1 and 491 living (Rose Bengal stained) individuals per 10 cm3 sediment volume (ind./10 cm3) along this transect with the highest standing stocks close to the saline spring (stations Sud C1-1 and C1-2; Fig. 4). The most dominant species were Entzia sp. (up to 194 individuals), Trochamminita salsa (up to 174 individuals) and Trochamminita irregularis (up to 167 individuals). Entzia macrescens, Miliammina fusca, and Haplophragmoides manilaensis were common or rare (Figs. 3, 4; Appendix 3). Between 30 and 663 ind./10 cm3 were observed in the dead assemblages, with the highest numbers at stations Sud C1-1 and Sud C1-2, again close to the spring. The most dominant dead species include Entzia sp. (up to 248 individuals), E. macrescens (up to 86 individuals), T. irregularis (up to 189 individuals), T. salsa (up to 68 individuals), M. fusca (up to 68 individuals), and H. manilaensis (up to 14 individuals). Siphotrochammina lobata and Haplophragmoides wilberti were rare in the dead assemblages.

Luisenhall Transect (Central Thuringia)

Soil water salinity at the Luis 1 transect in Luisenhall (central Thuringia) was low with values between 1.3 and 8.8 PSU (Fig. 5; Appendix 2). These values, however, should be treated with caution because of the low amount of water that was available for the measurements. Nonetheless, the salinities measured in the saline pond and ditch at Luisenhall were in a similar range (see Table 1). The pH values ranged from 7.4 to 7.7.

Up to 38 living G. arctica per 10 cm3 were found along this transect. It was the only living species recorded (Fig. 5). The total number of dead specimens ranged between 19 and 2051 ind./10 cm3. The most dominant species in the dead assemblages was again G. arctica (up to 1853 individuals), followed by E. macrescens (up to 127 individuals), T. irregularis (up to 36 individuals), and Entzia sp. (up to 29 individuals). Miliammina fusca, T. salsa, H. wilberti, and H. manilaensis were rare, and some juvenile trochamminids were found in low numbers (Appendix 3).

Artern Transect (Northern Thuringia)

The salinity along the Art 1 transect at Artern (northern Thuringia) ranged between 15.7 PSU in the sediments from the saline pond to 1.5 PSU in the soil water with increasing distance from the pond. The pH varied between 7.6 and 7.8 (Fig. 6; Appendix 2). We found up to 52 living ind./10 cm3 along the transect (Fig. 6). The live population comprised E. macrescens (with up to 47 individuals), Entzia sp. (up to 5 individuals), and Gordiospira arctica (one individual). Between 2 and 618 ind./10 cm3 were found in the dead assemblages. They were less diverse and clearly dominated by E. macrescens (with up to 569 individuals), followed by Entzia sp. (up to 32 individuals) and S. lobata (up to 10 individuals).

Auleben Transect (Northern Thuringia)

The soil water salinity at the Au 1 transect close to Auleben (northern Thuringia) showed values of up to 5.7 PSU. The pH had a low range and varied around 7.2 (Fig. 7; Appendix 2). The total number of living specimens was low with 0 to 9 ind./10 cm3 (Fig. 7). The populations comprised T. irregularis, S. lobata, E. macrescens, and G. arctica at stations Au 1-1 and Au 1-2. The total number of dead specimens ranged from 1 to 193 ind./10 cm3. The most dominant specimen was E. macrescens with up to 122 individuals, followed by T. irregularis (up to 28 individuals), Entzia sp. (up to 20 individuals), S. lobata (up to 10 individuals), and G. arctica (up to 5 individuals). Other taxa were present in low numbers in the dead assemblages. They include M. fusca, T. salsa, and juvenile trochamminids.

Esperstedt Transect (Northern Thuringia)

No soil salinity could be determined along Esperstedt Esp 1 transect from northern Thuringia due to the lack of soil sediment. The salinity in the nearby saltwater ditch was 17.7 PSU, and the pH was 8.4 (Table 1). The total number of living specimens (i.e., E. macrescens) was very low with 2 ind./10 cm3. They were found in one sample only (Esp 1-2; Fig. 8). The total number of dead specimens was also very low and ranged from 2 to 7 ind./10 cm3. Abundant taxa include E. macrescens with up to 3 individuals, T. irregularis with up to 2 individuals, and Entzia sp. with up to 3 individuals. Other species present in the dead assemblages comprised S. lobata, T. salsa, and juvenile trochamminids.

Benthic Foraminifera in the Other Samples

Benthic foraminifera were also found in almost all other surface samples, partly with a high species richness. In the five Sud A1 transect samples, which were taken at the northern Sülze bank in Sülldorf (Fig. 1), we observed live and dead E. macrescens, Entzia sp., G. arctica, and juvenile trochamminids as well as dead T. irregularis, M. fusca, S. lobata, and H. manilaensis. The sample inspection suggested that the foraminiferal density ranged from low to high.

In the three samples from transect Sud B1, located at an artificial branch of the Sülze River, the same species could be found, except for G. arctica, which was not present. Additionally, we observed live S. lobata and dead H. wilberti along this transect. The foraminiferal density was apparently low.

In one sample from transect Sud D1, taken in the brackish lake, no foraminifera could be found. The other three samples from this transect contained live and dead S. lobata, and dead Entzia macrescens, Entzia sp., H. manilaensis, G. arctica, and juvenile trochamminids. Foraminiferal density appeared to vary from high to very low.

The single sample from Dodendorf (Dod 1) in Saxony-Anhalt was dominated by E. macrescens, which was found living and dead. We also observed dead Entzia sp., and the foraminiferal density was relatively high. The single sample from Osterweddingen (Ost 1) in Saxony-Anhalt showed a low foraminiferal density. We observed only dead species of Entzia sp., H. manilaensis, and T. salsa.

One surface sample was screened from transect 2 near Esperstedt (Esp 2-2) from northern Thuringia. In sample Esp 2-2, live and dead Entzia sp. as well as dead E. macrescens and H. manilaensis were found. The foraminiferal density was rather low.

Along transects Luis 2 to 4 in central Thuringia, we generally observed low foraminiferal densities. In sample Luis 2-2 from transect 2, we found dead T. salsa and H. manilaensis. In sample Luis 3-2 from transect 3, we observed E. macrescens, Entzia sp., and H. manilaensis. In sample Luis 4-2 from transect 4, we found dead G. arctica, T. irregularis, H. wilberti, and juvenile trochamminids.

Live Population Dynamics in Central Germany

We found a high variability of the population densities between the different saline places in northern and central Thuringia as well as in Saxony-Anhalt. The total densities of live specimens are low at Esperstedt and Auleben with 2 to 8 ind./10 cm3, moderate at Luisenhall and Artern with 38 to 52 ind./10 cm3, and high at Sülldorf with up to 491 ind./10 cm3. These densities are much lower than those reported from a Danish salt marsh with standing stocks of up to 1548 ind./10 cm3 (Hunke, 2020). Even higher values of up to 8448 ind./10 cm3 were reported from a Portuguese salt marsh (Schönfeld & Mendes, 2022). The different population densities might be explained by the sampling date. At Sülldorf, the samples were taken in July 2022, and the other samples were taken in October 2022, probably reflecting a marked seasonality. Indeed, laboratory experiments showed no reproduction or low reproduction rates for intertidal and subtidal species at lower temperatures but higher reproduction rates at higher temperatures (e.g., Myers, 1936; Bradshaw, 1955, 1957; Muller, 1975; Salami, 1976; Kitazato & Matsushita, 1996; Goldstein & Alve, 2011; Saraswat et al., 2011). Field studies showed that some intertidal species had only one major reproduction event during the warm seasons (summer and fall) and that reproduction was low during the other seasons (Boltovskoy, 1964; Buzas, 1969; Reiter, 1959; Waldron, 1963; Murray, 1983; Alve, 1995). Horton & Murray (2007) showed a pronounced seasonal variation in standing stock of the intertidal zone of Cowpen salt marsh (UK) with a maximum in summer and a minimum in winter. By contrast, Saad & Wade (2017) observed a higher abundance of living foraminifera in September and October, another peak in May, and lower abundances in July and August on the Norfolk coast (UK). Bouchet et al. (2007) found a decline in foraminiferal population density in mudflats from the Bay of Biscay (Atlantic coast, France) under higher temperatures. They concluded that higher temperatures and diurnal temperature changes may result in higher remineralization of organic matter, which consumes oxygen, and, thus, high temperatures could be a limiting factor for reproduction. Others observed higher reproduction rates of intertidal and subtidal foraminifera related to higher food availability or algal blooms (Myers, 1942, 1943; Murray & Alve, 2000; Swallow, 2000; Debenay et al., 2006; Morvan et al., 2006; Schönfeld & Numberger, 2007). These observations suggest that not only temperature but also the availability of food may play a role for foraminiferal reproduction. Moreover, we observed that water salinities are strongly variable between seasons in Sülldorf, Dodendorf, and Osterweddingen. The salinity in the Sülldorf salt spring and brackish lake were 67.2 and 46.6 PSU in October 2022 (Table 1) but only 2.4 and 16.7 PSU in March 2023. Likewise, salinities in Dodendorf and Osterweddingen were 18.4 and 5.2 PSU in October 2022 and decreased to 3.5 and 1.3 PSU in March 2023. For a straightforward interpretation of the faunal dynamics in central Germany, a seasonal time series of soil salinities and temperatures is necessary.

Terrestrial Foraminiferal Assemblages in Central Germany in Comparison to Coastal Salt-Marsh Assemblages

We found dead intertidal foraminifera at all investigated saline habitats in central Germany. Differences in diversity and density were recognized among these localities. In general, we found the same species that are present in the live populations. When compared to the southern North Sea coastal salt marshes, we partly observed a higher species richness. At Sülldorf in Saxony-Anhalt, we found a highly diverse assemblage with Entzia sp., E. macrescens, T. irregularis, T. salsa, M. fusca, H. manilaensis, S. lobata, and H. wilberti in the dead assemblages. Agglutinated species such as T. irregularis, H. manilaensis, and H. wilberti have rarely been observed in natural and managed salt marshes along the southern North Sea coast (Lehmann, 2000; Gehrels & Newman, 2004; Müller-Navarra et al., 2016, 2017; Heinrich, 2020; Stoldt, 2020; Kremer, 2021; Nipper, 2021; Gothmann, 2022), in southern European salt marshes (Armynot du Châtelet et al., 2009; Leorri et al., 2010; Francescangeli et al., 2017; Schönfeld & Mendes, 2022), in subarctic salt marshes (Kemp et al., 2017), and salt marshes in South Africa (Strachan et al., 2016). In contrast, T. irregularis, H. manilaensis, and H. wilberti frequently occur in organic-rich salt marshes of the US-Pacific coast (e.g., Hawkes et al., 2010; Engelhart et al., 2013; Milker et al., 2015a,b), in salt marsh environments in the Gulf of Mexico region (Andersen, 1953), and at Bottsand Lagoon, Baltic Sea, Germany (Lehmann, 2000). Furthermore, Siphotrochammina lobata has been reported from a Swedish salt marsh by Lehmann (2000), but it has never been found in the southern North Sea or Baltic coastal regions. This taxon seems to prefer warm to temperate environments (Murray, 2006); it has been reported from salt marshes in Brazil, New England, North Carolina (USA; de Rijk & Troelstra, 1997; Eichler et al., 2007; Wright et al., 2011), and Portugal in sourthern Europe (Martins et al., 2015; Schönfeld & Mendes, 2022). Likewise, Trochamminita salsa has not been recorded in the southern North Sea coastal region to date. The species is nonetheless abundant in Australian and New Zealand salt marshes (e.g., Callard et al., 2011; King, 2021), in Chile (Jennings et al., 1995), in the Caribbean (e.g., Cushman & Broennimann, 1948; Saunders, 1957), and is also documented in rare occurrences in Louisiana and North Carolina (USA; Dreher, 2006; Vance et al., 2006) and in Portugal (Fatela et al., 2012).

In contrast to earlier studies on salt marshes in Europe, we found only one miliolid species, which was identified as G. arctica. This species was the most dominant species along transect 1 at Luisenhall. Gordiospira arctica has been reported from northeastern Greenland by Cushman (1933), in the shallow waters of the Arctic Sea by Loeblich & Tappan (1955), from shallow waters of the Laptev Sea (Lukina, 2001; Matul et al., 2007), from the outer Restigouche estuary in the Chaleur Bay (Canada; Schafer, 1973), and in inner-neritic Holocene records from Prudhoe Bay (Alaska; McDougall et al., 1986). Other species of this genus (i.e., Gordiospira fragilis) have been observed in shallow waters from Antarctica and in sediments from Subantarctic fjords (Majewski, 2005; Majewski et al., 2023). This geographical distribution suggests a preference of Gordiospira species to cooler climatic conditions. It could also be possible that Gordiospira is highly dissolution-resistant, because other calcareous taxa (Ammonia spp. and Elphidium spp.) have been reported from Holocene brackish lake sediments from Saxony-Anhalt (Wennrich et al., 2007; Fig. 1A). However, the soil water pH values at Luisenhall were in the range of 7.2 and 7.8 in the present study, which makes early taphonomic dissolution of calcareous tests less likely (e.g., Berkeley et al., 2007). We therefore consider that calcareous species other than G. arctica are recently not present at central German saline habitats. It is conceivable that this species benefits from higher salinities at Luisenhall. Soil salinity was highest with 8.8 PSU in October 2022 at station Luis 1-2 where the highest densities of live and dead G. arctica have been observed. Earlier measurements showed that soil salinities at Luisenhall can increase up to 40 PSU (Sparmberg et al., 2005). However, salinity alone cannot explain the dominance of G. arctica at Luisenhall, because it was not observed in other samples with high salinities, such as those from Sülldorf and Artern.

Dead foraminiferal densities in the studied areas are higher than those of the live populations and range between 1 and 2051 ind./10 cm3. Highest abundances were found close to Luisenhall (up to 2051 individuals), followed by Sülldorf (up to 662 individuals) and Artern (up to 618 individuals). The lowest abundances, with up to 194 and 7 ind./10 cm3, were recorded close to Auleben and Esperstedt, respectively. The highest abundances at Luisenhall were higher than densities in a salt marsh in Iceland where ca. 98 ind./10 cm3 have been found (Lübbers & Schönfeld, 2018). These values are generally in good agreement with abundances reported from salt marshes on German and Danish North Sea islands with 880 to 2636 ind./10 cm3 (Heinrich, 2020; Hunke, 2020; Nipper, 2021). However, the densities at Luisenhall were much lower than those of dead foraminiferal tests from an organic-rich salt marsh in Oregon (USA) with 27530 ind./10 cm3 (Milker et al., 2015b). Studies on Arctic and Subarctic salt marshes on Iceland and Svalbard suggested that the population densities were influenced by varying freshwater influx and hence pore- and seep-water salinity (Lübbers & Schönfeld, 2018; Golikova et al., 2022). Provided that the dead assemblage mirrors the living one, it is conceivable that higher population densities at some stations at Luisenhall, Sülldorf, and Artern may be due to higher soil water salinities at these stations, ranging from ∼8 to ∼16 PSU.

The relatively high densities and a considerably high number of species at Sülldorf, Luisenhall, and Auleben suggest stable assemblages that have been established for a long time. This is supported by our own observations. We did not find living or dead foraminifera in salt meadows with present Salicornia europaea close to the tailing pile Zielitz, north of Magdeburg, in March 2023. The salt mining began in 1973, and the first halophytic plants were recorded in 1985/1986 and more diverse halophytic flora in 1998 (Westhus & Westhus, 1998). Indeed, the first observations of foraminifera in saline habitats in central Germany have been made in Thuringia by Bartenstein (1939) and later by Rieth (1958). However, these studies have only reported occurrences of single species. Holocene records of a typical shallow-marine species of the genus Ammonia have been reported by Wennrich et al. (2007) from formerly brackish lakes in Saxony-Anhalt, suggesting their persistence for a period of several thousand years. It has been often assumed that foraminifera have been repeatedly transported into terrestrial saline habitats or lakes by migratory birds (e.g., Almogi-Labin et al., 1995; Wennrich et al., 2007), but it remains unclear from where they came to the inland sites. A provenance from the North Sea or Baltic Sea coasts and transport over the east Atlantic flyway is plausible (Fig. 9; Wennrich et al., 2007; van Roomen et al., 2022). Arctic regions have to be considered as well, in particular for G. arctica. Other taxa, for instance T. salsa and S. lobata, might have also been transported from southern Europe over the east Atlantic flyway (Fig. 9; van Roomen et al., 2022). In addition, more easterly migration routes and potential connections to the Adriatic Sea, eastern Mediterranean Sea, and Black Sea are also possible (Fig. 9; Spina et al., 2022).

The saline habitats in central Germany have been influenced by both natural saline springs and discharges related to potassium mining with known starting dates of mining and fertilizer processing. These dates could provide further insights into the colonization history and dynamics of foraminifera in the study area. However, information on how long it takes for foraminifera to colonize a new environment and to establish a stable, resilient assemblage are rare. The (re-)colonization rates of foraminifera in salt marshes are in the range of years (Cearreta et al., 2013; Masselink et al., 2017). A long-term monitoring of the tidal restoration of a salt marsh in Oregon showed that the first species re-recolonized the substrates ten months after tidal restoration and that stable assemblages were not yet established six years after tidal restoration (Milker et al., 2022). These examples, however, refer to coastal salt marshes, where the colonizing species occur in the direct vicinity and the recolonization did not require a long-distance transport.

A Hidden Foraminiferal Diversity in Central Germany?

A yet unrecognized Entzia sp. was dominant at Sülldorf and also occurred at other sites. This taxon showed some of the morphological features of E. macrescens (i.e., a closed umbilical region, one or more secondary apertures with a distinct lip on the final chamber, and a brownish test color. Entzia sp. differed from E. macrescens by having fewer (mostly seven) and inflated chambers in the final whorl, hence a more globular outline, a less distinct slit at the base of the final chamber, and a coarser agglutination. The grains were mainly from coarse, angular quartz that are flush with the test surface, and less than 10% needle-shaped or oval fragments of diatoms, which are irregularly arranged. They were not flush with the surface and broken off, creating lengthy voids on the surface (Figs. 3.1 to 3.4). Diatom fragments were missing in tests of E. macrescens found in this study. These features are in agreement with Rieth (1958), who reported that tests of “E. tetrastomella” from saline habitats at Artern contained broken pieces of diatoms. On the other hand, von Daday (1884) observed silicate plates in E. tetrastomella tests from a terrestrial salt marsh at Rumanian salt ponds. We further observed that only the earliest chambers of the specimens from Sülldorf collapsed during drying, while the entire tests of E. macrescens commonly collapse when drying (Bartenstein & Brand, 1938; Filipescu & Kaminski, 2011). Broennimann & Whittaker (1984) described a paralectotype of E. macrescens with more globular earlier chambers that partly match the Entzia sp. found in this study, even though the specimens illustrated (their figs. 1-12 to 1-15) had a finer-grained test. Kaminski et al. (2020) reported that larger specimens of E. macrescens from a salt marsh in Bahrain have a distinct tendency to have a lobate outline. Some of their specimens seem to have a slightly coarser-grained test (their plate 2) but match the other morphological features of E. macrescens. The Entzia sp. from central Germany mostly has one or two secondary apertures. von Daday (1883, 1884) described four secondary apertures for each individual of his E. tetrastomella. Bartenstein & Brand (1938) reported that their Jadammina polystoma always has three to seven secondary apertures in the Jade region in northern Germany. Our own and other observations (Gehrels, 1994; de Rijk, 1995) imply that not all specimens of E. macrescens (= J. polystoma) have secondary apertures, and, hence, the number of secondary apertures may not be considered as species-specific for the taxa of the genus Entzia (Gehrels & van de Plassche, 1999).

Holzmann & Pawlowski (2017) found that E. macrescens and E. tetrastomella specimens from salt marshes in Great Britain and Romania belong to the same genotype and form a monophyletic group. The genus name Entzia has therefore been given priority and has been extensively used since then. However, they also recorded a cryptic species of Entzia, which has been collected in the Camargue (southern France). The specimens were morphologically identical to E. macrescens, despite showing a markedly coarser-grained test (plate 1 in Holzmann & Pawlowski, 2017). This may be considered as evidence that a cryptic diversity of Entzia is morphologically expressed in their wall structure.

Since we were not able to find living specimens of Entzia sp. in October 2022 and March 2023 for a genetic analysis, we cannot state whether our taxon is identical to E. macrescens or represents a cryptic species within the genus Entzia. Schönfeld & Mendes (2022) noted that a comparison of topotypic gene sequences from the type locality (Jade Bight, Northern Germany) of J. polystomaBartenstein & Brand (1938) with the topotypic gene sequence of Entzia tetrastomellavon Daday (1884) is necessary to prove the validity of the genus Jadammina. Future genetic investigations from the studied and other German locations will allow a more detailed and comprehensive phylogenetic analyses to constrain the cryptic diversity in the genus Entzia.

Trochamminita salsa was dominant at Sülldorf as well (Figs. 3.13 and 3.16–3.18). The tests are planispirally to slightly irregularly coiled, have an open umbilical region, and show one to two secondary apertures or two connected sinusoidal apertures at the base of the final chamber. In contrast to earlier illustrations of T. salsa (Callard et al., 2011; King, 2021) and to the original description (Cushman & Broennimann, 1948), our specimens are relatively coarsely agglutinated. Corroborating evidence was provided by Saunders (1957) who noted that the coarseness of the test can vary considerably, and by Jennings et al. (1995) who imaged T. salsa with coarse-grained tests. On the other hand, shape and chamber arrangement of our specimens also compare well to T. irregularis (Fig. 3). However, the specimens do not show a basal slit as originally described for juvenile T. irregularis (Cushman & Broennimann, 1948). Furthermore, we observed that T. salsa specimens often collapsed during drying, which is not the case for Trochamminita species (King, 2021). Again, genetic investigations are necessary to assess the presence of different genotypes or to prove the high degree of morphological variability in T. salsa.

The most dominant species at Luisenhall is best identified as G. arctica, as it matches almost all characteristics described for the species and the genus Gordiospira in general (Cushman, 1933; Loeblich & Tappan, 1955, 1988). In summary, the tests are discoidal with an early streptospiral and later planispiral coiling; the wall is calcareous, light and milky white, thin and delicate. The test shows transverse growth stripes and an open-tube-like aperture at the end of the tubular chamber. The irregular coiling in the early and central part of the test is also characteristic. Cushman (1933) pointed out that the thinness of the wall is the major difference to species of the genus Cornuspira. In addition to the characteristics above, we observed a few smaller pseudopores at the inner part of the second tubular chamber that have, to our knowledge, never been described for G. arctica (Fig. 3.25). These pseudopores are not visible under a light microscope. All our specimens are very delicate and small―their diameter is on average 100 µm and, hence, much smaller than the specimens described in Loeblich & Tappan (1955) with maximum diameters between 390 and 880 µm.

All investigated terrestrial saline habitats in Thuringia and Saxony-Anhalt were inhabited by foraminifera usually reported from near-shore and intertidal environments. Nine different species and juvenile trochamminids, which could not be determined to species level, were recognized in the present study. The live populations as well as the dead assemblages were particularly diverse at Sülldorf in Saxony-Anhalt and at Luisenhall in Thuringia, where they are composed of intertidal foraminifera known to occur in the southern North Sea coastal region, in southern Europe and elsewhere.

We observed species that have not been described from southern North Sea salt marshes to date. Two species were previously known from southern Europe (S. lobata and T. salsa). The only miliolid taxon recorded in the present study, G. arctica, has been described from high northern latitudes. A yet unknown species, Entzia sp., occurred as the most dominant species at Sülldorf in Saxony-Anhalt. We conclude that foraminiferal assemblages in central Germany have been established over a long time, presumably since the early Holocene and that the different species were brought to central Germany via migratory birds on their way from South to North and vice versa. The recognition of Entzia sp. infers that the development of cryptic, endemic species may take place as well.

Genetic investigations, in particular barcoding of the species found at terrestrial saline habitats in central Germany and comparisons with sequenced specimens from the species’ type localities will allow a better understanding of their provenance, phylogenetic position, and population dynamics.

This study was carried out in the frame of the research project SEASTORM, which is part of the Priority Program (SPP-1889) ‘Regional Sea Level Change and Society (SeaLevel)’. Financial support was provided by grants MI1508/4-2 and SCHM1180/19-2 from the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG). We thank the students Olga Dressler and Tom Sill from the Universität Greifswald for the chemical water measurements in October 2022 and Pavel Reich for support in the field in July 2022. We further thank the Amt für Planung und Umwelt, Sachgebiet Naturschutz und Forsten, Landkreis Börde (Saxony-Anhalt) for a field work permit. The study is a contribution to the Center for Earth System Research and Sustainability (CEN) of Universität Hamburg.

APPENDICES

Appendix 1: Taxonomic List of the Species Identified in This Study.

Entzia macrescens (Brady) = Trochammina inflata (Montagu) var. macrescens Brady 1870, p. 290, pl. 11, fig. 5a–c

Entzia sp.; see chapter 5.3

Miliammina fusca (Brady) = Quinqueloculina fusca Brady 1870, p. 286, pl. 11, fig. 2a–c

Siphotrochammina lobata Sanders 1958, p. 9, pl. 3, fig. 1–2

Trochamminita irregularis Cushman and Broennimann 1948, p.17, pl. 4, figs. 1–3

Trochamminita salsa (Cushman and Broennimann) = Labrospira salsa Cushman and Broennimann 1948, p. 16, pl. 5, figs. 5–6; see also chapter 5.3

Gordiospira arctica Cushman 1933, p. 3, pl. 1, fig. 5–7; see also chapter 5.3

Haplophragmoides wilberti Andersen 1953, p. 21, pl. 4, fig. 7a–b

Haplophragmoides manilaensis Andersen 1953, p. 22, pl. 4, fig. 8a–b