Abstract

We studied the distribution and ecology of modern foraminifera in a salt marsh in the Bay of Tümlau, Eiderstedt peninsula at the German North Sea coast; this marsh is influenced by human activities. To encompass the full range of environments, we sampled natural and grazed salt marshes, and adjacent tidal flats for foraminiferal and environmental parameters, including salinity, pH, grain size, and elevation relative to the tidal frame. Agglutinated taxa Jadammina macrescens, Trochammina inflata, and Miliammina fusca, and the miliolid Quinqueloculina sp. dominate the vegetated salt marshes, however their distribution patterns lack a clear separation between low, middle and high marsh faunas. Tidal flats, tidal channels, marsh ponds and drainage ditches are characterized by hyaline species, among which Elphidium williamsoni is dominant in ponds, while Elphidium excavatum, Haynesina germanica, and Ammonia batava dominate tidal flats and ditches. The different marsh species occupy specific niches linked to ecosystem stability and the combined influence of submergence frequency, substrate (i.e., grain size), pH, and likely food sources. The observed lack of salt marsh foraminiferal subzones and the small-scale spatial variability of species distributions reflect the various impacts of diking, ditching, sheep grazing and sediment compaction on the morphology, hydrology and vegetation in the studied salt marsh. The faunas lack a consistent relation to elevation above sea-level, restricting the applicability of foraminiferal reference data sets from human-interfered salt marshes for past sea-level reconstructions.

INTRODUCTION

Salt marshes represent the transition zone between terrestrial and marine ecosystems and are characterized by strong physical, biogeochemical and biological gradients (Allen, 2000). Many salt marshes are increasingly altered by local human influences such as land reclamation, diking, and grazing. In this context, a better understanding of the stability and resilience of salt marsh ecosystems to human interference and ongoing sea-level rise appears essential (Kirwan & Megonigal, 2013).

Benthic foraminifera are abundant in salt marshes worldwide and their tests are readily transferred into the sedimentary archive. The distribution patterns of salt marsh foraminifera in naturally developed coastal intertidal environments are closely related to gradients in salinity, pH, grain size, and tidal range, allowing for the characterization of different ecological niches (e.g., Bradshaw, 1968; Scott & Medioli, 1978, 1986; Alve & Murray, 1999; Edwards et al., 2004b; Wright et al., 2011). These gradients are, in turn, closely related to the distance from the coast and hence, to the tidal frame. Accordingly, salt marsh foraminifera show a distinct vertical zonation relative to the tidal frame (Scott & Medioli, 1978; Gehrels, 1994; Horton et al., 1999a) making them precise indicators for past relative sea-level changes. In this context, transfer functions have been developed to quantify the relationship between modern foraminifera and tidal level (Barlow et al., 2013; Kemp & Telford, 2015), which are then applied to foraminiferal assemblages in fossil records (e.g., Guilbault et al., 1995; Edwards et al., 2004a; Gehrels et al., 2006a, 2012; Horton & Edwards, 2006; Kemp et al., 2013b).

In coastal wetlands influenced by human activities, the hydrodynamic conditions, morphology and ecological zonation of salt marshes can be severely altered due to the impact of ditches and dikes (Vincent et al., 2013). However, little information is available on the foraminiferal fauna from these altered ecosystems. The distribution of foraminifera in human-influenced salt marshes seems to mainly be controlled by salinity (De Rijk, 1995; De Rijk & Troelstra, 1997). Salt marsh ecosystems along the southeastern North Sea coast have experienced a long history of human interferences including diking and land reclamation since medieval times, and transfer to pastures accompanied by intense ditching and poldering (Meier, 2004). The distribution of foraminifera in a largely natural-grown salt marsh in Ho Bugt, western Denmark exhibited a zonation closely related to tidal elevation and pH, while salinity appeared less important (Gehrels & Newman, 2004). The small-scale patchiness and population dynamics of foraminifera were studied in a salt marsh of the Schleswig-Holstein west coast by Lehmann (2000). This study revealed three main foraminiferal assemblages associated with specific vegetation units and confined to the lower, middle and upper supralittoral line. The faunas exhibited significant species-specific spatial and seasonal changes in standing stock and test size, likely responding to the seasonal temperature and vegetation cycle.

The present study provides the first detailed inventory of foraminifera from a German North Sea salt marsh and adjacent tidal flat ecosystems in the Bay of Tümlau (Germany). The studied salt marsh has experienced poldering, ditching and dike construction in the past, and parts are still impacted by sheep grazing, altering the natural elevation profile and vegetation succession. We hypothesize that these anthropogenic impacts influence foraminiferal distribution patterns and vertical faunal zonation. We also aim to test if modern faunas from this area can serve as reliable reference data sets for the reconstruction of past sea-level changes based on fossil faunas from regional salt marsh sediment archives.

STUDY AREA

The salt marsh is located in the Bay of Tümlau on Eiderstedt peninsula, North Frisian coast of the German North Sea (Fig. 1). The coastal wetlands are part of the Schleswig-Holstein Wadden Sea National Park, which was founded in 1985 and became an UNESCO world heritage site in 2009. The Bay of Tümlau itself is a remnant of a former tidal stream (Ehlers, 1988).

The Holocene coastal evolution of the southeastern North Sea is related to post-glacial sea-level rise and isostatic vertical movements (Gehrels et al., 2006b; Vink et al., 2007). In more recent times, the natural development of the North Frisian coast has been influenced by tidal inundations, and erosion and re-deposition during storm surges. Due to severe flooding events, which frequently affected the coast during the past centuries, the coast has been successively diked for coastal protection and land reclamation purposes since <1100 AD (Meier, 2004; Dangendorf et al., 2014). The diking resulted in an alteration of the hydrological conditions of the salt marshes (van der Molen, 1997), and various ancient tidal flat areas have become dry land. The most recent dikes at the Bay of Tümlau were built in 1933 and since then the local salt marsh developed its present shape. In addition to diking, the salt marshes were ditched for land reclamation by developing a network of drainage systems, which partly ended in 1998 (Stock et al., 2005). Since then, natural silting of the drainage systems has occurred. Within the salt marshes, isolated, stagnant, un-vegetated ponds have developed. Besides the artificial drainage system, naturally meandering tidal channels drain the marsh area (Fig. 1).

The Bay of Tümlau has an astronomical tidal range of 1.52 m with distinct semidiurnal tides. Mean high water (MHW) reaches 0.69 m relative to mean tide level (MTL; reference tide gauge “Tümlauer Hafen”; Fig. 1), mean low water (MLW; based on four nearby tide gauges) reaches −0.83 m relative to MTL. According to data from the Schleswig-Holstein Agency for Coastal Defense, National Park and Marine Conservation (ACNM-SH), the elevation of the investigated salt marsh ranges between 0.31 m in ditches and tidal channels, and 1.28 m on the vegetated salt marsh, which is 64% of the tidal range. Most parts of the salt marsh are only submerged during storm floods with mean heights above 1.24 m or partly during highest astronomical tides (HAT) with mean heights of 1.23 m relative to MTL (Fig. 2). Records from the Federal Maritime and Hydrographic Agency (BSH) document that landward winds (295° ± 90°) increase the water level at the German North Sea coast while seaward winds (109° ± 90°) decrease the water level. Most of the storm floods occur during the winter season and are related to strong westerly winds. The climate of the area is temperate-humid with cold to mild winter months with a mean temperature of 5.2°C and mild summer months with a mean temperature of 13.4°C (weather station Elpersbüttel, survey duration: 1994–2005; German Meteorological Service). Seawater salinity at the Bay of Tümlau is lowest during winter (between 23 and 24 psu) and highest during summer (29–30 psu; BSH, survey in 1995).

The salt marsh of the Bay of Tümlau mainly consists of low marsh environments with a few patches of high marsh (Fig. 1b). The low marsh is characterized by vascular plant associations comprising Triglochin maritima Linné, Plantago maritima Linné, Atriplex portulacoides Linné, Limonium sp., and Agrostis stolonifera Linné. The high marsh areas are characterized by vascular plants such as Artemisia maritima Linné, Carex extensa Goodenough, Elymetum atherici Pellizzari, Merloni and Piccoli, and Juncus geradii Loiseleur-Deslongchamps. The low marsh/tidal flat transition is sparsely vegetated with Salicornia europaea Linné, Puccinella maritima (Hudson) and Spartina sp. (Stock et al., 2005).

MATERIAL AND METHODS

Surface sediments were sampled along three transects (D, E, F) across the salt marsh of the northeastern Bay of Tümlau in April 2013 (Fig. 1). Transects were installed in the ditched salt marshes and cover a range of intertidal habitats (i.e., tidal flats to salt marsh environments). Our new data set is accompanied by a previous study (Ottmar, 2012) based on a sampling campaign in March 2011 in the northwestern Bay of Tümlau (A, B, C; Fig. 1). The results of Ottmar (2012) mainly refer to faunas from the tidal flat, marsh ponds and ditches, and thus we use it for evaluation of the whole range of foraminiferal habitats in the discussion chapter.

A total of 43 surface sediment samples were collected along Transects D, E, and F using a metal frame measuring 10 cm × 10 cm length by 1 cm depth for foraminiferal analysis (Appendix 1). All samples were preserved in a rose Bengal solution (2 g rose Bengal per liter, 96% ethanol) on the sampling day to separate living (rose Bengal stained) individuals from dead (unstained) individuals (Walton, 1952). Additional surface sediment samples were taken for salinity and pH measurements, and grain-size analyses. Measurements of salinity and pH samples were performed corresponding to the standard DIN ISO 10390: 2005-12. For this purpose, 10 g dry sediment of each sample were shaken for one hour in 25 ml demineralized water, and subsequently the solution rested for one hour. The measurement was performed in the suspension using a hand held multi-meter (Multi 340i Set). Samples for grain-size analysis were treated for a couple of weeks with H2O2 to dissolve the organic content. Grain-size analyses were performed with a diffraction particle-size analyzer (Sympatex HELOS/KF Magic), using apertures of 0.5–3500 μm.

All sites were surveyed with a manual leveling system, referring to a geodetic reference point approximately 1 km east of the sampling area (UTM32 WGS84: 477968 E, 6027295 N; Fig. 1B). Heights relative to MTL were calculated using laser scan data of the salt marsh surface obtained in 2010 by LKN-SH (Schleswig-Holstein’s Government-Owned Company for Coastal Protection, National Parks and Ocean Protection).

After determination of the wet volume, samples were wet-sieved over 500 μm and 63 μm sieves to separate larger organic particles (>500 μm) and material smaller than 63 μm. The 63–500 μm residue of each sample was split into equal aliquots using a wet splitter after Scott & Hermelin (1993). The samples were counted wet because drying of samples may result in under-representation of fragile agglutinated species (e.g., Scott & Medioli, 1980b; De Rijk, 1995). All stained and non-stained benthic foraminifera were counted under a stereo-microscope until a minimum number of 200 non-stained tests were found. Only tests with bright red staining were considered alive at the time of collection (Murray & Alve, 2000). The residues >500 μm were examined for foraminifera before being disregarded. The identification of the foraminiferal taxa was mainly based on the publications of Hofker (1977), Gehrels & Newman (2004), and Horton & Edwards (2006) (Appendix 2). For documentation purposes, images from most of the modern species were created using a Zeiss Leo VP 1455 scanning electron microscope.

For the multivariate statistical analyses, we used dead assemblages to integrate seasonal and temporal fluctuations in the populations (e.g., Buzas, 1968; Murray, 1982; Horton, 1999; Murray & Alve, 2000). For classifying the general distribution of the salt marsh fauna, we applied a hierarchical clustering method. To define groups (clusters) on the basis of the mean distance between objects in each group, we used the unweighted pair group average (UPGMA) algorithm. The distance metric was selected according to the cophenetic correlation, which is the linear Pearson correlation between the original matrix and the dissimilarity matrix (e.g., Legendre & Birks, 2012). We finally used the Chord dissimilarity (Overpeck et al., 1985) distance measure, which is a common metric for quantitative community data (Simpson, 2012). Cluster analysis was carried out with the PAST software package, version 2.15 (Hammer et al., 2001).

Detrended Correspondence Analysis (DCA; Hill & Gauch, 1980) was performed to test whether species in the modern samples exhibit a unimodal or linear response along an environmental gradient. The test revealed a gradient length of 2.4 standard deviation (SD) units (first axis), indicating a more unimodal species response (Birks, 1995). Consequently, Canonical Correspondence Analysis (CCA; Ter Braak, 1986), based on a unimodal species-environment relationship was used to further analyze the relationships between the foraminiferal species and the environmental parameters elevation, salinity, pH, and grain size [silt and clay = mud (<63 μm) content]. A data set containing only species with a relative abundance of <1% in at least two samples was used in the analyses and environmental parameters were standardized. For both DCA and CCA, we used the software package CANOCO, version 4.5 (Ter Braak & Smilauer, 2002; Leps & Smilauer, 2003).

We calculated the Pearson coefficients between the environmental parameters (grain size, salinity, pH, elevation) and species relative abundances to determine the linear (inter) correlations between the biotic and abiotic factors using the PAST software package, version 2.15 (Hammer et al., 2001).

RESULTS

Environmental Parameters

The elevation of the tidal flat stations ranges between 0.31–0.94 m and the elevation of the salt marsh stations is 0.97–1.28 m relative to MTL in the study area. At sample sites of Transects D, E, and F, pore-water salinity varied from 1.71–12.74 (Fig. 2; Appendix 1). Higher salinities (4.03–12.74) were measured in the tidal flat and lower salinities (1.71–8.06) in the salt marsh. In the tidal flat, pH varied from 8.05–8.18 while in the salt marsh, pH varied from 7.54–8.14 and generally decreased landwards. Typically, the salt marsh environments are characterized by muddy substrate (mud content 41.5–98.3%), and the tidal flat environments by sandy to muddy substrate (mud content 32.6–75.1%) (Fig. 2).

Foraminiferal Distributions

Standing stocks of live specimens were <10 individuals/10 cm3 at all sites. The most abundant live taxa include Jadammina macrescens and Quinqueloculina sp. in the salt marsh of Transect D [Station (St.) D1–D13] and Haynesina germanica in the mudflat of Transect F (St. F14, F15).

A total of 30 different foraminiferal taxa, partly grouped by genus, were distinguished in the dead fauna. The higher salt marsh (St. D1–D11, E1–E8, F1–F9) is dominated by the miliolid Quinqueloculina sp., and the agglutinated taxa J. macrescens, Miliammina fusca and Trochammina inflata. The tidal flat and lower salt marsh environments (St. D12–D16, E9–E12, F10–F15) are dominated by the hyaline H. germanica, Elphidium excavatum, Elphidium williamsoni, and Ammonia batava (Figs. 2, 3). Associated abundant taxa (3–10% of the total fauna) of salt marsh and tidal flat environments are Ammonia cf. beccarii, Nonion depressulum, and Nonion sp. 1, while rare taxa (with <3 % of the total fauna) include Balticammina pseudomacrescens, Bolivina spp., Bolivina variabilis, Bulimina spp., Buliminella borealis, Cibicides spp., Cornuspira involvens, Paratrochammina haynesi, Stainforthia fusiformis, Textularia spp., Tiphotrocha comprimata, and Trochammina ochracea (Appendix 3).

In the higher parts of the salt marsh, relative abundances of agglutinated taxa are 76–87% for J. macrescens, 1–34% for T. inflata and 1–23% for M. fusca (Fig. 2). The relative abundances of the calcareous Quinqueloculina sp. increase with increasing distance from the coastline and exhibit a maximum of 40% at Transect F (St. F3; Fig. 2). The abundances of other calcareous taxa (mainly H. germanica, E. excavatum, E. williamsoni, and A. batava) range from 0–40% in the higher salt marsh with some local peak occurrences at St. D2, D5, E3 and F3 and increasing towards the tidal flat (Fig. 2).

In the tidal flat, channels and lower parts of the salt marsh, H. germanica, E. excavatum, E. williamsoni and A. batava are the dominant taxa and comprise 40–68% of the total fauna counted. Elphidium williamsoni and H. germanica have a relative abundance of up to 16% and 68%, respectively. The occurrence of E. excavatum is mainly restricted to the tidal flat and lowermost salt marsh environment (St. E10–E12, D14–D16, F10–F15) where it comprises 10–46% of the total fauna. Ammonia batava also commonly occurs in the tidal flat and lowermost salt marsh (St. D14–D16, E10, E11, F11–F15), with relative abundances of up to 10%. None of the species show a strong linear correlation to elevation, with R values of −0.49–0.42 (Appendix 4).

Results of the Multivariate Statistical Analyses

Cluster analysis revealed two main clusters, representing the separation between salt marsh and tidal flat faunas (Fig. 4). Cluster I contains nearly all stations from higher marsh environments, with elevations of 0.97–1.26 m relative to MTL, and mainly comprises the salt marsh taxa J. macrescens, T. inflata, M. fusca, and Quinqueloculina sp. Cluster II contains all mud flat and lowest marsh stations, and higher salt marsh Station D5, with elevation of 0.31–1.28 m relative to MTL. This cluster is characterized by the hyaline taxa H. germanica, E. excavatum, E. williamsoni, A. batava, and N. depressulum (Fig. 4).

The first axis of the CCA analysis explains 33% and the second axis explains 4.3% of the total variance of the data set. Both axes are significant at the 95% confidence level (p-value <0.05). Substrate and elevation are negatively related and pH is positively related to the first axis, salinity is positively related to the second axis (Fig. 5). The calcareous species E. excavatum and H. germanica (and to a lesser extent, A. cf. beccarii and N. depressulum) and the agglutinated species P. haynesi (and to a lesser extent Textularia spp.) are positively related to pH and negatively related to mud content of the substrate and to elevation. Agglutinated taxa J. macrescens and T. inflata are positively related to both elevation and mud content. Cornuspira involvens, Quinqueloculina sp. and M. fusca show a positive correlation to mud content and salinity, and A. batava, S. fusiformis and Cibicides spp. (and to a lesser extent E. williamsoni and T. ochracea) to salinity and pH (Fig. 5).

DISCUSSION

Ecology of Salt Marsh and Tidal Flat Faunas

Benthic foraminifera, especially agglutinated species, in naturally developed salt marshes commonly exhibit a close relationship to the tidal frame, as it is shown for salt marshes worldwide (e.g., Scott & Medioli, 1978; Scott & Leckie, 1990; Gehrels & Newman, 2004; Horton & Edwards, 2006; Hawkes et al., 2010; Kemp et al., 2012; Engelhart et al., 2013; Milker et al., 2015b). This zonation reflects the specific gradients created by the diurnal tidal submergence, and related physical, biogeochemical and biological parameters. In this respect, the distribution of the different foraminiferal species is controlled by the specific requirements and tolerance levels to substrate type, pH, elevation with respect to the tidal frame, and to a lesser extent, salinity (Horton et al., 1999b, 2000; Edwards et al., 2004b; Gehrels & Newman, 2004; Horton & Murray, 2007). The natural morphology of the salt marsh in the Bay of Tümlau has been distorted by ditching and related drainage (see discussion below; Figs. 1, 6). As a consequence, the salt marsh faunas lack a clear relationship to the tidal frame (Fig. 2, 4). Instead, the CCA identified substrate type (grain size) and pH, as well as elevation, as the most important environmental parameters (Fig. 5).

The majority of hyaline species were restricted to the tidal flat and lower marsh environments, where they are positively related to pH and negatively related to muddy substrate and elevation. In the Bay of Tümlau, E. excavatum, H. germanica and A. batava dominate the sandier substrates in the lowest marsh and tidal flat, where an average pH of 8.1 and salinities of up to 14 psu were recorded. However, in this environment, salinities can reach up to 30 psu during the summer months (BSH, survey in 1995). These species also occur in tidal channels and artificial ditches in the Bay of Tümlau (Ottmar, 2012; Fig. 6). They are known to tolerate a wide range of salinities but appear sensitive to heavy metal and hydrocarbon pollution (Armynot du Châtelet & Debeney, 2010). These species are characteristic of shallow-marine environments of the southern North Sea (Jarke, 1961; Murray, 1992) and are also typical for the German Bight and near-coastal ecosystems under estuarine influence (Wang, 1983; Schönfeld et al., 2013). Ammonia batava and closely related Ammonia tepida are very common in organic-rich littoral and coastal settings (Alve & Murray, 1999; Hayward et al., 2004; Armynot du Châtelet et al., 2009) and are able to survive and reproduce even under oligohaline (1.2–1.5 psu) conditions (Wennrich et al., 2007). Elphidium excavatum occurs with different morphotypes in a wide range of shelf and coastal habitats of the Arctic, North Atlantic, North Sea, and Baltic Sea (Feyling-Hanssen, 1972; Schönfeld & Numberger, 2007). This species has also been recorded from near-shore sands and intertidal marshes (summary in Feyling-Hanssen, 1972) and from the western Baltic Sea, where its main reproductive cycle was related to feeding and growth during the spring bloom (Schönfeld & Numberger, 2007). Haynesina germanica has been recorded in low marsh environments with salinities of up to 35 psu in Chichester Harbour, UK (Swallow, 2000). In the near-coastal ecosystems of the southeastern North Sea, H. germanica shows some affinity to estuarine influence (Wang, 1983), which may also explain its persistence in some salt marsh sites of the Bay of Tümlau (Fig. 2). A dominance of this species at higher elevation relative to A. tepida and E. excavatum was also documented in Aiguillon Cove on the French Atlantic coast (Armynot du Châtelet et al., 2009).

Elphidium williamsoni is a common species of the tidal flat in the Bay of Tümlau (Fig. 2), but also occurs in the salt marsh. In the western part of the Bay of Tümlau, this species was found to be dominant on relatively sandy substrates in stable ponds on the salt marsh, where it constitutes up to 90% of the total foraminiferal assemblage (Ottmar, 2012; Fig. 6). The CCA results suggest a negative relationship of E. williamsoni to mud content and positive relation to salinity (Fig. 5), but other factors such as specific food sources may also play a role. A similar correlation of E. williamsoni to sandy substrate and salinity was previously reported from an estuarine environment in southwestern Spain (Ruiz et al., 2005).

Agglutinated species J. macrescens and T. inflata, which occur in high numbers in the salt marsh (Figs. 2, 6), are positively related to elevation and muddy substrate and negatively related to pH (Fig. 5). Both species are cosmopolitan (e.g., Hawkes et al., 2010; Engelhart et al., 2013; Fatela et al., 2014; Hayward, 2014) and are associated with marsh plants. Specifically, J. macrescens flourishes epiphytically on decaying Carex leaf debris (Alve & Murray, 1999). In the Bay of Tümlau, highest abundances of these species appear in the vegetated and high marsh areas, which are inundated only during storm floods and often exhibit particularly low pH values. Trochammina inflata can live at the extreme limits of tidal influence (Hayward, 1993) and has been observed in the higher marshes of the North American Pacific and Atlantic coasts (Hawkes et al., 2010; Engelhart et al., 2013; Kemp et al., 2013a). It has also been found on the North Sea coast of the UK where it inhabits the high and middle marshes (Horton & Murray, 2007). Laboratory experiments indicate a grain-size dependency of T. inflata, with a relation to silty substrates (Matera & Lee, 1972).

Quinqueloculina sp. and M. fusca are also found in the salt marsh environments of the Bay of Tümlau, where they are positively correlated to muddy substrate and occur within a salinity range of 3–8 psu (Figs. 2, 4, 5). Both taxa seem to favor the same microhabitat with an affinity to muddy substrate (Lee et al., 1969). Commonly, the relative abundances of Quinqueloculina sp. and M. fusca exhibit a slight landward increase, however, elevated numbers can also be observed locally in lower marsh environments (Fig. 2). Similar distribution patterns have also been reported from other regions (e.g., Gehrels, 1994; De Rijk & Troelstra, 1997; Kemp et al., 2013b). Alve & Murray (1999) described M. fusca as typically representative of the seaward edge of salt marshes. Miliammina fusca has been reported from high and middle marsh environments from a salt marsh in the UK (Swallow, 2000; Horton & Murray, 2007), from low marsh and tidal flat environments along the US Pacific coast (Jennings & Nelson, 1992; Hawkes et al., 2011; Engelhart et al., 2013; Milker et al., 2015a, b) and from tidal flat environments of New Zealand (Hayward, 1993). These studies mentioned salinity as the main controlling factor of this species.

Taphonomy and Fossilization Potential of Foraminiferal Faunas

The loss of calcareous specimens can influence the accuracy of sea-level estimates when a modern data set, including calcareous species, is applied to fossil samples where the calcareous species have been dissolved. In the study area, calcareous species dominate the tidal flat, but also occur in different salt marsh environments, where they account for up to 40% of the foraminiferal fauna, and are even more abundant in marsh ponds of the western Bay of Tümlau (Ottmar, 2012). Early diagenetic dissolution of calcareous tests has been observed in many salt marshes (e.g., Scott & Medioli, 1980a; Horton et al., 1999b; Berkeley et al., 2007, 2009; Hawkes et al., 2010; Engelhart et al., 2013; Milker et al., 2015a, b) and has been attributed to pH values lower than 7.2 (Berkeley et al., 2007). Laboratory experiments revealed that at a pH of 5.0, complete dissolution of calcareous tests occurred within one day, and identified a pH window of 2 to 9.5 at which some foraminifers can exist (Bradshaw, 1968). In our study area, pH values were always higher than 7.2, and in seaward direction, pH increased to values above 8 in April 2013. Similar values were measured in March 2011 in the western Bay of Tümlau (Ottmar, 2012). The relatively high pH values relative to naturally developed salt marshes is likely a reflection of the intense ditching and grazing that prevents the development of a natural vegetation succession and related acidification of salt marsh soils. Hence, the pH range in the study area does not affect foraminiferal test dissolution and favors the occurrence and long-term preservation of calcareous taxa in subsurface salt marsh sediments.

The fossilization potential of agglutinated foraminiferal taxa is influenced by physical destruction of tests by wave action during storm flood events, repeated drying of empty tests, compaction, or by bacterial degradation of test cement in subsurface sediments (e.g., Goldstein et al., 1995; Goldstein & Watkins, 1999; Culver & Horton, 2005). Tests of Jadammina macrescens appear particularly prone to degradation, as indicated by decreasing numbers in subsurface sediments from the Fraser River delta, British Columbia (Jonasson & Patterson, 1992). In other salt marsh areas, agglutinated tests have been reported to be well preserved (e.g., Scott & Medioli, 1980b, 1986). High rates of test degradation have also been documented for M. fusca (Goldstein & Watkins, 1999; Murray & Alve, 1999), while tests of T. inflata appear to be more robust (J. Gauthier, pers. comm.). Based on preliminary results from sediment cores from the Bay of Tümlau, agglutinated taxa proved to be well preserved in subsurface sediments, indicating a high fossilization potential for these foraminifera in our study area.

Small-Scale Spatial Variability of Salt Marsh Foraminifera

The integration of our results with those of an earlier study (Ottmar, 2012) allows for an assessment of small-scale spatial differentiation of environments and foraminiferal assemblages in the Bay of Tümlau salt marsh. The salt marsh meadows are internally subdivided by artificial ditches and natural ponds, the latter being particularly frequent in the northwestern part of the study area (Fig. 1B; Ottmar, 2012). The marsh pond assemblages mainly consist of E. williamsoni and E. excavatum that are even more abundant in the ponds than in the adjacent tidal flats. Notably, E. williamsoni is most dominant in the ponds sampled along transects A and B (Fig. 1B), where it accounts for up to 90% of the total assemblage and exhibited unusually high standing stocks of up to 160 live individuals per 10 cm2 in March 2011 (Ottmar, 2012). The high numbers of E. williamsoni in the ponds can be attributed to the specific feeding strategy of this species. Lopez (1979) documented a higher uptake rate of chloroplasts by E. williamsoni relative to E. excavatum. Obviously, E. williamsoni benefits from the rich and stable algal communities that are present in marsh ponds. The ditches and natural tidal channels are also inhabited by hyaline taxa, mainly by E. excavatum and H. germanica (Ottmar, 2012). In the ditches, both taxa are related to relatively sand-rich substrates, free of vegetation, similar to conditions in the tidal flat environments.

These findings are relevant for future sampling strategies, particularly with respect to naturally developed, unditched salt marshes, where the number of ponds is usually much higher when compared to ditched marshes (LeMay, 2007). The documented small-scale differences have a direct influence on the quantitative interpretation of modern assemblages and establishment of transfer functions for sea-level reconstructions. In future studies, these issues could be addressed by a wider spatial sampling, instead of sampling along single transects, in order to capture all microhabitats. In addition, lateral shifts of channels and ponds are likely documented in sediment cores and related faunas, which may result in erroneous sea-level estimates.

Anthropogenic Impacts on the Distribution of Foraminifera

The foraminiferal distribution patterns in the Bay of Tümlau reflect the specific morphology of the salt marsh, which lacks the usual landward increase in elevation but instead slightly rises towards its seaward end (Fig. 2). The local salt marsh was ditched around 1900 for land reclamation purposes and ditches are still visible as linear features (Fig. 1B); some areas now have developed naturally as part of nature reserves. To the landward side, the salt marsh is further bordered by a dike, which protects the hinterland from storm floods. The dike prevents the lateral migration of the salt marsh and thus the development of a natural succession with a low, middle, and high marsh. As a consequence, only a few high marsh and middle marsh areas can be found (Stock et al., 2005) and the transition to the tidal flat is regularly represented by erosional edges.

These processes, superimposed by the compaction of the muddy substrate of the salt marsh by desiccation and capillary suction stress (Brain et al., 2011), modified the hydrology of the salt marsh and the drainage process. Further drying following rare flooding events (only during HAT and storm floods) has resulted in subsidence of older parts and an overall concave cross profile with rising edges (LeMay, 2007; Stock, 2011). Similar processes and morphologies have been documented for ditched salt marsh areas along the northeast American coast (Vincent et al., 2013). Accordingly, only two main foraminiferal zones were observed in the Bay of Tümlau, including a lowest marsh/ tidal flat zone, and a salt marsh zone lacking a clear subzonation with respect to the tidal frame. The salt marsh zone is predominantly inhabited by agglutinated species, represented by Cluster I. The tidal flat and lowest marsh zone is inhabited by hyaline taxa, represented by Cluster II (Fig. 4). The artificial alteration of the salt marsh morphology for drainage results in a distortion of the tidal frame, so that the salt marsh is only submerged during HAT and storm floods (van der Molen, 1997). Consequently, the foraminiferal distribution in the Bay of Tümlau is not primarily controlled by diurnal tidal submergence and, hence, elevation is similar to that previously described by De Rijk & Troelstra (1997) for a ditched salt marsh in Massachusetts (USA). These authors mentioned pore water salinity as an important parameter acting on the foraminiferal distribution in these human-altered salt marshes.

Sheep grazing in parts of the salt marsh in the Bay of Tümlau has resulted in a reduction of the floral diversity, accompanied by reduced trapping of suspended sediment (Stock, 2011), and likely an alteration of the biogeochemical processes in the soils. The grazed parts of the salt marsh (particularly at Transect D) are dominated by a monospecific Agrostis stolonifera community. However, it seems that this monospecific plant community does not have any influence on the foraminiferal distribution in the study area because their distribution along transect D is similar to that of the other transects (Fig. 2). Comparable monospecific grass communities are typical for grazed marshes (Kiehl et al., 1996). Interestingly, this grass species is still dominant in some of the currently protected and non-grazed areas of Transects E and F. This suggests an extensive recovery period for natural floral secondary succession (Kiehl et al., 1996).

The ditching, diking and grazing processes altered the salt marsh morphology in the Bay of Tümlau, preventing the development of distinct floral and foraminiferal zones in equilibrium with the tidal frame (Fig. 6). To date, the natural zones have not yet established in areas that have not been grazed for at least several years. Our results confirm the study of De Rijk & Troelstra (1997) and Mills et al. (2013), who concluded that the topography plays a crucial role for the vertical zonation of intertidal foraminifera relative to the tidal frame. A tight and distinct vertical zonation is restricted to salt marshes with a regular landward-rising topography (Scott & Medioli, 1980b). As a future perspective, regular monitoring of benthic foraminiferal and floral successions in the Bay of Tümlau would be useful to assess the recovery potential of human-altered salt marshes, and to provide information on the response of these ecosystems to the impact of sea-level rise.

CONCLUSIONS

We investigated the modern foraminiferal distribution in human-influenced salt marsh environments of the Bay of Tümlau at the German North Sea coast. Based on cluster analysis, two main foraminiferal assemblages were distinguished: an internally undifferentiated salt marsh assemblage dominated by the agglutinated species J. macrescens, T. inflata and M. fusca and the miliolid Quinqueloculina sp., and a lowest marsh/tidal flat assemblage dominated by the hyaline species H. germanica, E. excavatum, and A. batava. Canonical Correspondence Analysis revealed that the foraminiferal distribution is mainly influenced by substrate type, pH and elevation, and to a lesser extent by salinity. Among the most common species, H. germanica, E. excavatum and A. batava are mainly related to higher proportions of sand in the sediments and to higher pH values, while J. macrescens, T. inflata, M. fusca and Quinqueloculina sp. are mainly related to finer-grained substrate and lower pH. In contrast to naturally developed salt marshes, pH did not drop significantly below 7.5 in the tidal flat and salt marsh areas in the Bay of Tümlau. Consequently, greater preservation of calcareous species is evident compared to more natural salt marshes. The morphology, hydrology and vegetation of the salt marsh in the Bay of Tümlau has been significantly altered by human influence, including ditching and sheep grazing, the landward dike for coastal projection, and by sediment compaction. As a consequence, the salt marsh has a weakly developed concave morphology with rising edges, thus lacking a continuous landward rise in elevation and associated foraminiferal and vegetation zonation. Our results demonstrate that single transects of modern benthic foraminiferal samples in human-interfered salt marshes, particularly with a small elevation range, do not provide reliable reference data sets for the establishment of transfer functions and application in sea-level reconstructions. The presence of ditches, tidal channels, and ponds creates a high level of small-scale variability of ecosystems and associated foraminiferal faunas within the salt marsh. This underlines the need of a wider spatial sampling to record all microhabitats in anthropogenic-influenced salt marshes.

ACKNOWLEDGMENTS

We thank Martin Stock and the administration of the Schleswig-Holstein Wadden Sea National Park for providing the permission to enter the protected zones of the Bay of Tümlau. We thank Matthias A. Ottmar, Helge A. Winkelbauer and Ole Valk for their support in the field, providing of data and fruitful discussions. We are grateful to Marc Theodor for his kind assistance in the realization of the SEM photos. We thank Mareike Paul, Jutta Richarz, Eva Vinx, and Helge A. Winkelbauer for their support in the laboratory. The manuscript greatly profited from thorough reviews by Jason Kirby and an anonymous reviewer. We appreciate the suggestions of the editor, Pamela Hallock, and her assistant editor, Rebekah Baker. The German Research Foundation DFG is thanked for financial support through the Cluster of Excellence CliSAP (Integrated Climate System Analysis and Prediction).

APPENDIX 1

APPENDIX 2

APPENDIX 3

Census data of total (live + dead) benthic foraminifera in the 63–500 μm size fraction of the studied transects D, E, and F. This table can be found on the Cushman Foundation website in the JFR Article Data Repository (http://www.cushmanfoundation.org/jfr/index.html) as item number JFR_DR2016002.

APPENDIX 4

Pearson correlations (R) and p values between foraminiferal species and abiotic factors in the Bay of Tümlau. This table can be found on the Cushman Foundation website in the JFR Article Data Repository (http://www.cushmanfoundation.org/jfr/index.html) as item number JFR_DR2016002.