Review of Palaeobotany and Palynology 186 (2012) 22–37

Contents lists available at SciVerse ScienceDirect

Review of Palaeobotany and Palynology

j ourna l homepage: www.e lsev ie r .com/ locate / revpa lbo

Research paper

Expanding NPP analysis to eutrophic and forested sites: Significance of NPPsin a Holocene wood peat section (NE Germany)

Alexandra Barthelmes a,⁎, Pim de Klerk b, Anja Prager a, Martin Theuerkauf a,Martin Unterseher a, Hans Joosten a

a Institute of Botany and Landscape Ecology, Ernst-Moritz-Arndt-University, Grimmer Straße 88, D-17487 Greifswald, Germanyb Staatliches Museum für Naturkunde Karlsruhe, Erbprinzenstraße 13, D-76133 Karlsruhe, Germany

⁎ Corresponding author. Tel.: +49 3831 864179; fax:E-mail address: abarthelmes@gmx.de (A. Barthelme

0034-6667/$ – see front matter © 2012 Elsevier B.V. Alldoi:10.1016/j.revpalbo.2012.07.007

a b s t r a c t

a r t i c l e i n f o

Article history:Received 10 January 2012Received in revised form 11 July 2012Accepted 12 July 2012

Keywords:non-pollen palynomorphsalder carrfungal sporesHolocenetaphonomyNE Germany

Alnus glutinosa-dominated peatlands are widespread in central Europe, but the generally bad preservation ofmicro- and macrofossils has hampered palaeoecological research of their peats. Because of its large carbonsequestration rate, however, peat accumulation in forested peatlands is of special interest for climate change re-search. This study identifies indicator groups for various types of alder (A. glutinosa) carr and sedge (Carex) fenvegetation, elaborated by analysis of non-pollen palynomorphs (NPPs) from peat and surface samples. The indi-cator value of fungal spores and decomposition products of wood was tested by correlation with pollen (espe-cially ALNUS) and macrofossils. Only few indicators of alder carr also occurred with low and constant valuesduring distinct open sedge fen phases, which indicates that small and plane shaped NPPs can be dispersedextra-locally. The diversity and abundance of NPPs appeared to depend on vegetation type and resulting nutrientsupply and to water regime and resulting decomposition intensity during peat development.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

Forests dominated by Alnus glutinosa have been present in CentralEurope since the Early Holocene (Lang, 1994; Berglund et al., 1996).At present, A. glutinosa has a Euro-Siberian distribution. In Europe, itis only absent from northern Scandinavia, the central and easternparts of the Iberian Peninsula and parts of Greece (Meusel et al.,1965). In Northeast Germany, A. glutinosa is widespread in peatlands,where alder wood peat is also abundant. Because of the predominant-ly bad preservation of fossils, only few studies (Marek, 1965; Brown,1988; Waller, 1993, 1994; de Klerk et al., 1997; Pokorný et al., 2000;Barthelmes et al., 2006) have addressed the palaeoecology of aldercarrs. Due to their rapid sequestration rate and large carbon storage(Dommain et al., 2011), however, forested peatlands are of special in-terest in climate change research (Barthelmes, 2009).

Inclusion of non-pollen palynomorphs (NPPs, ‘types’ sensu vanGeel, 1972), especially fungal spores, has in the last decades substan-tially progressed palynological research (van Geel and Aptroot, 2006).Spores of coprophilous fungi were recognised as indicators of herbi-vores and grazing intensity (e.g. Bos et al., 2005; Davis and Shafer,2005; Blackford et al., 2006; Graf and Chmura, 2006; Cugny et al.,2010; Feeser and O'Connell, 2010; Ejarque et al., 2011), whereasother spores appeared to provide useful information on fire andwoodland disturbance (Blackford and Innes, 2006; Innes et al.,

+49 3831 864114.s).

rights reserved.

2010) or on the conditions of bogs (Yeloff et al., 2007) and lakes(Kramer et al., 2010). Fungal spores also facilitated the reconstructionof human activity and environmental change in archaeological re-search (e.g. van Geel et al., 2003; Mighall et al., 2006).

Despite the widespread use of NPPs, the knowledge on their taxo-nomic identification and the distribution and ecology of the inferredspecies is still very poor (Blackford et al., 2006). Furthermore, the eco-logical interpretation of the NPP record sometimes conflicts with thatof the associated micro- and macrofossil assemblages (Ryan andBlackford, 2010; Wood and Wilmshurst, 2011). Our knowledge offungal NPPs has to be improved urgently, e.g. through surface samplestudies along gradients of fen types (Prager et al., 2006, 2012–thisissue), grazing intensity (Blackford and Innes, 2006) or other abioticparameters (Mulder et al., 2003).

Fungi growing on decaying wood, roots, litter and living trees(Michael and Henning, 1967; Ellis and Ellis, 1997) and remnants ofincompletely decomposed wood (Odier and Monties, 1983; Bauer,2004) may provide valuable indicators in alder carrs. Some NPPshave indeed been attributed to fungal species that may decomposewood, like HDV-7A (ascospore of Chaetomium), HDV-44 (ascosporeof Ustulina deusta), HDV-112 (ascospore of Cercophora), HDV-143(ascospore of Diporotheca rhizophila), HDV-172 (ascospore ofConiochaeta cf. ligniaria), HDV-359 (fungal spores), HDV-360 (sporeof cf. Brachysporium) or represent wood fragments, like HDV-114(scalariform perforation plate; van Geel, 1978; Pals et al., 1980; vanGeel et al., 1980/81; Bakker and van Smeerdijk, 1982; van der Wiel,1982; van Geel et al., 1982/83; van Geel and Aptroot, 2006), but

23A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

only a few studies have until now focussed on NPP analysis of eutro-phic and forested sites (Barthelmes et al., 2006; Prager et al., 2006).

While Prager et al. (2006) presented very preliminary results,Prager et al. (2012–this issue) process the complete data and conclu-sions from an extensive surface sample study of NE German fen veg-etation and elaborate distinct indicator values of NPPs. All relatedpapers of Prager et al. and Barthelmes et al. introduce several newEMA-types with detailed morphological descriptions and exhaustiveecological interpretations. Barthelmes et al. (2006) used the prelimi-nary data from Prager et al. (2006) to reconstruct peatland develop-ment of a highly decomposed wood peat section from NE Germany.Our paper aims to improve the indicative value of NPPs by combiningthe latest results from this surface sample study with that of an untilnow unpublished fossil wood peat section. This methodological workwill support the interpretation of NPP assemblages (esp. of NPPsderiving from fungal spores and plant tissue) and highlights somespecial challenges of their application in palaeoecology.

2. Material and methods

2.1. Sample collection

The alder wood peat section HBG (Hoher Birkengraben) originatesfrom the 110 ha large Endinger Bruch fen in Northeast Germany

Fig. 1. Location of study site En

(Fig. 1; N 54°14′45″, E 12°53′04″) (de Klerk, 2002). The EndingerBruch is recently dominated by alder carrs and sedge fens. A 445 cmalder wood peat section was obtained with a ‘Usinger corer’(100 cm length, diameter 8 cm; Mingram et al., 2007). Palynologicalsamples were taken with an interval of ca. 10 cm.

2.2. Microfossil analysis

Sample preparation (Fægri and Iversen, 1989) included treatmentwith HCL, 20% KOH, sieving (120 μm) and acetolysis (7 min).Counting was carried out with a Zeiss axiolab light-microscope with400× magnification; larger magnifications were used for the identifi-cation of problematic pollen grains.

In order to separate clearly between observed palynomorphologicalentities and inferred taxa, the former are displayed in the text in SMALL

CAPITALS (Joosten and de Klerk, 2002). Palynomorphological entitieswere named following the keys used for identification. Pollen andplant spore types were identified with Moore et al. (1991) (indicatedwith the epitheton ‘m’ in Fig. 2), and the Northwest European PollenFlora (Punt, 1976; Punt and Clarke, 1984; Punt and Blackmore, 1991)(‘p’, in Fig. 2). ‘MONOLETE SPORES WITHOUT PERINE’ includes Polypodiaceaespores without perine.

Pollen and NPP values were calculated relative to a sum of pollentypes attributable to upland trees and shrubs (AP) and upland herbs

dinger Bruch (core HBG).

24 A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

(NAP). BETULA, SALIX and FRAXINUS were included, although their pro-ducers may occur locally in alder carrs, because their inclusion didnot affect the calculated percentages (Janssen, 1959).

A catalogue (including digital photos) of all recurrent and distinctNPP types was elaborated. Description of the new NPP types strictlybases on morphological features (size, shape, number and character-istics of apertures and appendices, wall colour, surface structure) asobserved during this study (Barthelmes, 2009). Description of surfacestructure and apertures follows Moore et al. (1991). Names of NPPsinclude a three letter code for the laboratory where the relevantNPP was first identified: e.g. HDV for Hugo de Vries Laboratory Am-sterdam or EMA for Ernst-Moritz-Arndt University Greifswald(Barthelmes et al., 2006; Prager et al., 2006).

From the 150 NPP types distinguished we used 41 (9 HDV- and 32EMA-types) for further interpretation. These types are clearlyrecognisable, occur in large quantities and/or have distinct indicationvalues in the surface samples of Prager et al. (2012–this issue).

The fossil NPP data were comparedwith those from 55 surface sam-ples collected in nine alder carrs, one birch carr and three sites withopen fen vegetation in Northeast Germany. These sites differed withrespect to mean water level, water regime (e.g. amplitude of waterlevel fluctuation) and vegetation type (Prager et al., 2012–this issue).

2.3. Macrofossil analysis

Macrofossil samples were taken at selected depth levels to repre-sent the phases of fen development indicated by the microfossil data.Samples (25 cm3) were boiled in KOH (10 min) and sieved into fourfractions: >1 mm, 0.5–1 mm, 0.2–0.5 mm and b0.2 mm. Sample vol-umes were determined with water displacement. Samples wereanalysed with a binocular type MBC 10 (USSR) with magnificationsof 0.6–70×, and with a Zeiss axiolab light microscope with magnifica-tions of 400×.

Macrofossil typeswere identifiedwithKac andKac (1933), Beijerinck(1947), Kac et al. (1965), Nilson andHelmquist (1967), Berggren (1969),Grosse-Brauckmann (1972), and Grosse-Brauckmann and Streitz(1992).Alnus-typewoodwas identified by examination of referencema-terial. Wooden rootlets are non-herbaceous rootlets, whereas fibres ofwood are remains of decayed wood. Herbaceous rootlets include allnon-wooden radicles (Fig. 2).

Fossil diaspores are expressed as absolute numbers per sample,plant tissues as volume percentages relative to the total sample vol-ume before processing. Volume percentages were estimated in stepsof 5% in each single fraction and subsequently calculated for thetotal volume. This paper only presents data on plant tissues andsum curves of diaspores. For the complete macrofossil record and in-terpretation, see Barthelmes (2009).

2.4. Data processing and statistics

Calculations and presentation of palynological data were performedwith TILIA 2.0.b.4 and TGVIEW 2.0.2 software (Grimm, 1992, 2004).The resulting diagram (including pollen, macrofossils, NPPs) wasstratigraphically ordered and zoned with Constrained Cluster Analysis.

An additional unconstrained Detrended Correspondence Analysis(DCA, Pcord Version 4) was used to address the heterogeneity withinzones HBG-B2 and HBG-D). We used log values to accommodate forthe wide range of abundances (10−1 to 103%).

2.5. Regression analysis was done with Microsoft® Excel 2002

2.5.1. DatingAMS-radiocarbon dating of five samples from core HBG resulted in

four reliable ages (HBG 45, 205, 255, 325 cm; Table 1; Barthelmes,2009) that were calibrated into calendar years using CALIB rev. 5.0.1

(Stuiver and Reimer, 1993, 2005) with the intcal04 calibrationdataset (Reimer et al., 2004).

3. Results

3.1. Fossil record of core HBG (Endinger Bruch)

The 15 m deep core comprises a Lateglacial section of silt gyttja(embedding a layer of detritus gyttja), a section of Holocene detritusgyttja, and wood peat (De Klerk, 2002). The results in this paper coverthe last part of the gyttja and the entire wood peat section.

Zone HBG-A (500–435 cm) largely comprises gyttja deposits.Samples are characterised by low percentages of pollen types as-cribed to peatland herbs and trees (e.g. THELYPTERIS PALUSTRIS, ALNUS,CICUTA VIROSA, CYPERACEAE; Fig. 2). Characteristic NPP types includebasal cells of hairs of Nymphaeaceae (HDV-127), Gloeotrichia type(HDV-146), leaf spines of Ceratophyllum (HDV-137) and cf. part ofNymphaeaceae (EMA-136). In the last sample (HBG 440 cm) peaksof THELYPTERIS PALUSTRIS, MONOLETE SPORES WITHOUT PERINE and increasingpercentages of CICUTA VIROSA, ASTER TYPE and CYPERACEAE reflectterrestrialisation of the coring site as is also apparent from the pres-ence of peat from a depth of 450 cm onwards (Fig. 2).

Subzone HBG-B1 (435–355 cm) shows strongly increased valuesof THELYPTERIS PALUSTRIS, ALNUS, CICUTA VIROSA, CYPERACEAE and FRAXINUS

EXCELIOR TYPE (Fig. 2). Abundance and diversity of NPPs have sharply in-creased, especially of fungal spores (cf. conidium of Excipulariafusispora EMA-36, ascospore of cf. Sphaeriaceae EMA-64, probably co-nidium of Melanconis alni EMA-3, ascospore of cf. Hypoxylon EMA-24,unknown fungal spore EMA-27, unknown fungal spore EMA-32 andascospore of cf. Diporotheca rhizophila HDV-143) and wood tissue re-mains (EMA-16, EMA-9 and EMA-7). Up to a depth of 400 cm dia-spores of light demanding species occur (Fig. 2).

In zone HBG-B2 (355–255 cm) most NPP types from the previoussubzone continue to occur, but with distinctly fluctuating values(Fig. 2). The pollen record shows similar fluctuating percentages ofALNUS, POACEAE: WILD GRASS GROUP, MONOLETE SPORES WITHOUT PERINE andTYPHA LATIFOLIA. A high number of diaspores from light demanding spe-cies were recorded in the first samples of the subzone.

In zone HBG-C (255–195 cm) percentages of ALNUS and of mostNPP types regularly recorded in HBG-B have considerably decreasedand the amount of NPPs is comparatively low (Fig. 2). Pollen curvesof POACEAE: WILD GRASS GROUP, MONOLETE SPORES WITHOUT PERINE andCYPERACEAE show distinct peaks.

In zone HBG-E (195–40 cm) ALNUS pollen reaches 75–100% (exceptsamples HBG 180 cm and HBG 112 to 80 cm, Fig. 2). The fossil spec-trum is largely dominated by NPPs derived from wood tissue, e.g.EMA-9, EMA-7 (both remnants of highly decayed wood), EMA-15,EMA-140 (both fragments of scalariform perforation plates) andHDV-114 (scalariform perforation plate).

3.2. Detrended Correspondence Analysis (DCA)

DCA of NPPs was carried out to assess the similarities of sampleswithout stratigraphical constraints and to deduce more detailed in-formation on vegetation and site conditions during peat develop-ment. Axis 1 of the ordination biplot explains 47% of theheterogeneity in the data set, axis 2 an additional 18%. Axis 3 can beneglected (Fig. 3).

Extremes of axis 1 are mainly determined by NPP types related tolake conditions (Nymphaeaceae, Ceratophyllum, algae and sponges, cf.EMA-136, EMA-137; HDV-127, HDV-137, HDV-146, HDV-424) or tosedge fen vegetation and associated conditions (EMA-131 and -132derived from Cyperaceae tissue, Fig. 3B). The main differences existthus between lake samples HBG 500 to 450 cm depth and the subse-quent peatland samples (Fig. 3A).

Fig. 2. Fossil record of core HBG (“Hoher Birkengraben”, Endinger Bruch area, selected curves only). Presented pollen types are all excluded from the upland pollen sum, and displayed as actual values (black silhouette curves) and with a5-time exaggeration. Relative frequencies of non-pollen palynomorphs are based on an upland pollen sum and presented as real values (histograms). Macrofossil silhouette curves (grey) represent real values (volumes in % 25 cm³) and a5-time exaggeration. Sum curve light demanding species include diaspores of inferred taxa Alisma plantago-aquatica, Carex appropinquata/paniculata, C. elata, C. pseudocyperus, C. riparia, Cicuta virosa, Eleocharis, Eupatorium cannabinum,Hippuris vulgaris, Hydrocharis morsus-ranae, Lemna, Menyanthes trifoliata, Mentha, Nymphaea, Oenanthe aquatica, Peucedanum palustre, Ranunculus flammula, R. lingua, Rumex hydrolapathum, Typha latifolia, and Utricularia (Ellenberg et al.,1992; light values ≥7). For nomenclature: see text.

25A.Barthelm

eset

al./Review

ofPalaeobotanyand

Palynology186

(2012)22

–37

Fig. 2 (continued).

26 A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

NPP types that strongly determine axis 2 (Fig. 3B) include at theone side among other the alder carr indicators EMA-27, EMA-32,EMA-36 and EMA-134, but also EMA-39 (indicative for grass-likeplants), EMA-68 (indicative for cormophytes) and EMA-91 (indica-tive for very wet open vegetation, Prager et al., 2012–this issue).The other end of axis 2 is determined by negative scoring of wood tis-sue remains HDV-114, EMA-15 and EMA-140 (the latter two beingdecomposition remains of HDV-114, Plate I.7; 29). Placed close tothem are tissue remains of wood (EMA-62, Plate I.15) or vascularplants (EMA-1), conidia of Alysidium resinae, a fungus occurring ondead wood (EMA-56, Plate I.14) and HDV-225.

3.3. Interpretation and discussion

3.3.1. Indicator values of non-pollen palynomorphs: modern vegetationvs. peat record

Several EMAs identified in the surface sample study of Prager et al.(2012–this issue) were also found in wood peat of core HBG. The fos-sil NPP record was largely dominated by wood tissue remains andfungal spores. The fungal spore NPPs largely belonged to fungi associ-ated with above-ground vegetation: plant pathogens and endophytes(Phaeosphaeria, Melanconis alni; Sieber et al., 1991), coprophilousfungi (Sporormia and Sporormiella; Ahmed and Cain, 1972) and

27A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

saprobes of coarse and fine woody debris (Hypoxylon). Fungi of therhizosphere, like root pathogens, mycorrhizal species and Dark Sep-tate Endophytes (for DSE see Jumpponen & Trappe, 1998) werescarce, despite the presence of a large amount of root and rhizomeremnants in the samples.

3.3.2. Fungal NPPs related to alder carrsPrager et al. (2012–this issue) identified more than 30 NPP types

indicative for recent alder carr habitats, including more than twentyderived from fungi (mainly spores and fruit body remains) and sever-al derived from wood tissue. Of these types, EMA-3 (conidium ofMelanconium state Melanconis alni), EMA-24 (ascospore of cf.Hypoxylon), EMA-36 (cf. conidium of Excipularia fusispora), EMA-59(fungal spore or conidiophore fragment), EMA-64 (ascospore, proba-bly of Sphaeriacea) occurred with high values only in alder carr zones(HBG-B and less pronounced HBG-D, Fig. 2) which affirms their valueas indicators of alder carrs in palaeostudies.

The fossil occurrence of HDV-112 (ascospore of Cercophora) has – incombination with archaeological site information – often been used asan indicator for the presence of animal dung in the surroundings ofthe sample site (van Geel and Aptroot, 2006). Occurrence of this NPPtype during wetland phases with high percentages of ALNUS (Fig. 2)and without anthropogenic indicators (Barthelmes, 2009) points, how-ever, at the sometimes disregarded affinity of several Cercophora spe-cies to decaying wood, culms, stems and leaves (Ellis and Ellis, 1997).

EMA-44 occurred in surface samples both in alder carr and in openvegetation (Prager, pers. comm.). Its sole occurrence in zones HBG-Band -D suggests that it is a stronger indicator of alder carrs thanthat of open fen vegetation (Fig. 2).

EMA-56 (conidium of Alysidium resinae, Plate I.14), is one of thefew exceptions that display higher values in the more decomposedsection HBG-D than in HBG-B, where most fungal NPPs have maxi-mum values (Fig. 2). A. resinae is a fungus occurring on decayingwood (Ellis and Ellis, 1997) and might point to heavy degradationof wood on the mire surface (Table 2).

The following fungal NPP types occurred with high values only dur-ing alder carr phases (zones HBG-B and ‐D), but were not recorded inthe surface samples: EMA-80 (fungal spore, resembles spores ofBrachysporiella setosa), EMA-133 (ascospore of cf. Sphaeriaceae) andEMA-135 (ascospore of cf. Valsaria foedans). Brachysporiella setosa, spe-cies of Sphaeriaceae and Valsaria foedans are fungi primarily occurringon decaying wood (Ellis, 1959; Breitenbach and Kränzlin, 1981) andmight be indicative of forested fen vegetation.

3.3.3. Fungal NPPs related to open fen vegetation or grass-like host plantsOf the clear open fen indicators identified by Prager et al. (2012–this

issue) only EMA-91 (cf. ascospore of Ceriophora palustris) occurred

Table 1Results of AMS-14C‐dating of core HBG and their calibration.

Sample name Depth level Dated material Lab. no.(cm)

HBG 45 44–45 Rubus, Urtica (diaspores) Poz-049

HBG 205 204–205 Alnus, Apiacea, Lycopus Menyanthes,Mentha (diaspores); leaf fragments

Poz-849

HBG 255 254–255 Alnus, Carex, Galium, Urtica (diaspores) Poz-849

HBG 310 309–310 Alnus, Carex, Menyanthes (diaspores);leaf fragments

Poz-849

HBG 325 324–325 Alnus, Carex, Menyanthes (diaspores) Poz-849

a According to Telford et al. (2004).

during sedge fen phase HBG-C but also (with higher abundance) inalder carr HBG-B (Fig. 2). Ellis and Ellis (1997) described C. palustris assaprobic on dead leaves of Carex acutiformis, C. paniculata, C. pendulaand C. riparia, of which the first two are common in alder carrs of NEGermany (Clausnitzer, 2004). Against expectation, we found alsoHDV-126 (hyphopodium of Clasterosporium caricinum) to be moreclosely associated with past Alnus dominated vegetation than withopen sedge fen (high values especially in zone HBG-B, Fig. 2). This par-adox might be explained by the special conditions prevailing in carrs.C. palustris and C. caricinum regularly occur as pathogens on variousCarex species, including C. acutiformis and C. riparia (Ellis and Ellis,1997). C. acutiformis is quite common and tends to be dominant in theherb layer of alder carrs of NE-Germany (Clausnitzer, 2004). Underincreased nitrogen availability plants may have an increased suscepti-bility to pathogenic fungi (Strengbom et al., 2005), in particular inpeatlands (Wiedermann et al., 2007). Alnus glutinosa lives in symbiosiswith nitrogen (N)-fixing Frankia bacteria that assimilate molecularN2 from the atmosphere (Akkermans and van Dijk, 1981) to an annu-al amount of 75 to 164 kg N2 ha−1 yr−1 (Binkley et al., 1992;Klingensmith and Vancleve, 1993), causing nitrogen enrichment ofthe site. Litter of alder trees is nitrogen-rich (Dawson and Funk,1981) and easily degradable (Irmler, 1995) due to its low C/N-ratio(Schaeffer and Schachtschabel, 1992), which results in a rapid nutrientturn-over (Wiebe, 1998) and in easy access to nitrogen. C. palustrisand C. caricinum (HDV-126) may thus have a larger preference forC. acutiformis in alder carrs compared to Carex species in open sedgefens. As Carex species do not or scarcely flower under the shady condi-tions prevailing in alder carrs (Wiebe, 1998), HDV-126 and EMA-91mayindicate the occurrence of Cyperaceae in alder carrs also in absence ofCYPERACEAE pollen.

In surface samples EMA-39 was found in both open vegetation andalder carr (Prager et al., 2012–this issue), whereas in core HBG thetype prevailed in the alder carr zone HBG-B (Fig. 2). EMA-39 is as-cribed to Phaeosphaeria sp., a highly specialised parasitic fungus ongrass-like plants (Shoemaker and Babcock, 1989). Higher abundancesof this NPP in alder carrs than in sedge fens probably again reflectsthe enhanced susceptibility of herbs to pathogen fungi under theN-enriched conditions of Alnus dominated sites (cf. HDV-126, EMA-91,see above).

3.3.4. Tissue-NPPs deriving from herbaceous plantsHDV-127 (basal cells of hairs of Nymphaeaceae), EMA-137

(cf. part of Nymphaeaceae epidermis, Plate I.27), EMA-136(cf. part of Nymphaeaceae, Plate I.28) and HDV-137 (leaf spinesof Ceratophyllum) reflect the existence of open water with standsof water lilies and hornwort during the lake phase of zone HBG-A(Fig. 2).

Age Age ; 1σ confidence interval Age in cal BP; weightedaverage of the probabilitydistribution functiona

(14C yr BP) (cal BP)

4 4070±50 4483–44424625–45124788–4763

4593

5 5880±50 6647–66446749–66516773–6767

6699

6 6160±50 7033–70027037–7156

7062

8 6290±40 7223–71747258–7232

7215

9 6510±50 7355–73327389–73737478–7415

7416

Fig. 3. A: DCA-biplot of samples. Wetland zones of core HBG are indicated with separate symbols. B: Cluster analysis of fossil samples; C: DCA-biplot of fossil samples and NPPs.Triangles indicate samples (see panel A).

28 A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

Some tissue remains derived from sedges were not recorded in thesurface samples, but occurred commonly in the fossil record, includ-ing EMA-131 (basal cells of Cyperaceae rootlets; Fig. 2; 8.u, z) andEMA-132 (epidermis of Cyperaceae; Fig. 2; 8.v). Their occurrence(Fig. 2) is independent from that of macrofossil type herbaceous

rootlets (that probably also derives from Cyperaceae). The macrofos-sil and pollen record of zone HBG-C reflects open sedge vegetation(see above; Fig. 2; Barthelmes, 2009), whereas EMA-131 andEMA-132 conspicuously decrease from the last samples of zoneHBG-B to the beginning of HBG-C, possibly because of taphonomical

29A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

reasons. EMA-131 and EMA-132 probably are decomposition prod-ucts of rootlets from herbaceous plants (e.g. of Cyperaceae) andtherefore occur mainly in the stronger decomposed peat of zoneHBG-B 2 rather than in the well preserved peat of zone HBG-C. Highabundances of these NPP types reflect the occurrence of Cyperaceaein a fen and low (or strongly fluctuating) water levels, as are typicalof most alder carrs (Wiebe, 1998; Clausnitzer, 2004). In well pre-served sections of sedge fen peat these types are rare because theCyperaceae rootlets remain largely preserved (zone HBG-C, HBG330 and 90 cm; Fig. 2).

3.3.5. Tissue-NPPs deriving from trees and shrubsPredominantwood tissue remains of the alder carr zones HBG-B and

HBG-D were EMA-7, EMA-8 (both remnants of highly decayed wood,Plate I.7; 8), EMA-9 (decayed hardwood periderm, Plate I.4), EMA-16(hardwood periderm) and EMA-62 (sclerenchymatic fibres ofdecomposed wood, Plate I.15), whereas HDV-114 (scalariform perfora-tion plate in vessels of hardwood), EMA-15 (fragment of HDV-114,Plate I.7) and EMA-140 (corroded HDV-114, Plate I.29) only occurredwith high values in zone HBG-D (Fig. 2; see below).

Whereas Prager et al. (2012–this issue) were not completely sureabout the indicator value of the wood tissue remains EMA-7, EMA-8and EMA-9, they here appear clearly related to alder carr deposits(Fig. 2). In the surface sample study EMA-62 reached its highestvalues in dry alder carrs with mean annual water levels far belowthe peatland surface (Prager et al., 2012–this issue). In the surfacesamples HDV-114 and EMA-15 occur associated with alder or birch,especially with dead wood of alder (Prager et al., 2012–this issue).EMA-140 probably only originates under heavy decomposition, e.g.due to low or fluctuating water levels.

These wood tissue remains probably stem directly from alder oralder dominated vegetation. But they may also be produced insedge fen phases from decomposing wood that is still lying on themire surface (stemming from a previous carr) or (probably on asmall scale) from vertically ingrowing tree roots (stemming from alater carr). Both processes may obscure the expected correlation be-tween wood tissue remains and tree pollen. More or less continuousrecords of some wood tissue NPP types that did not run parallelwith alder carr phases were also found in other wood peat sections(Barthelmes, 2009).

3.3.6. Other NPPsWe additionally found NPPs well known from gyttja deposits or

eu- to mesotrophic open water, including HDV-424 (Spongillidaespicules, Kuhry, 1997) and HDV-146 (Gloeotrichia type; van der Wiel,1982; zone HBG-A, Fig. 2). EMA-1 (tracheids of vascular bundles) indi-cates the presence of cormophytes (Prager et al., 2012–this issue) andHDV-225 was previously found in eutrophic to mesotrophic openwater and ephemeral pools (van Geel et al., 1989).

3.3.7. Wetland development reflected by non-pollen palynomorphsBased on stratigraphy, pollen and macrofossils from the core

HBG we could distinguish a lake phase (HBG 500–435 cm, Fig. 2),one prolonged and two short phases of sedge fen (HBG 255–195 cm; HBG 330 and HBG 90 cm) and two prolonged periods ofalder carr (HBG 435–255 cm; HBG 195–40 cm). Sedge fen vegeta-tion is reflected by conspicuously low ALNUS pollen percentages,peaks of CYPERACEAE and/or MONOLETE SPORES WITHOUT PERINE and the oc-currence of several diaspores from light demanding species (Fig. 2;for detailed interpretation based on the complete dataset seeBarthelmes, 2009). Below we assess to what extent these findingsare supported and/or improved by the NPP record.

3.3.8. Lake phase (HBG-A; 500–435 cm)The NPP record of zone HBG-A suggest a continuously high water

level, eutrophic to mesotrophic conditions and lake vegetation. The

record includes remains of Nymphaeaceae and Ceratophyllum(EMA-136, EMA-137; HDV-127, HDV-137; Fig. 2) accompanied bysponges (HDV-424) and cyanobacteria (HDV-146; van Geel et al.,1982/83; Kuhry, 1997). Generally, NPPs in lake sediments encompassa wide range of taxa (including green algae, cyanobacteria, macro-phytes, testate amoebae) that offer valuable ecological information(Smol et al., 2001). In contrast, pollen often reflects vegetation poorly(Zhao et al., 2006) due to prevailing vegetative reproduction (e.g.Ceratophyllum) and entomophily (e.g. Nymphaea). In the upper sam-ples of zone HBG-A (460 and 450 cm, Fig. 2) final terrestrialisation ofthe site is indicated by decreasing percentages of remains of water lil-ies (EMA-137, HDV-127) and sponges (HDV-424). The rising numberof NPP types from HBG 460 to 440 cm (Fig. 4) is probably attributableto the nearby expansion of Alnus glutinosa and the associatedextralocal input of related NPPs (see below), while the site was stillcovered by shallow water. These differences in the NPP assemblagesof zone HBG-A are also clearly illustrated in the DCA (Fig. 3A). Pollentypes like THELYPTERIS PALUSTRIS, CICUTA VIROSA, MONOLETE SPORES WITHOUT

PERINE, TYPHA LATIFOLIA and CYPERACEAE do not reflect the change fromlake to peatland until HBG 440 cm (Fig. 2).

3.3.9. Alder carr phase HBG-B (435–255 cm)The vast majority of NPP types consist of fungal spores (mainly

wood decomposer) and wood tissue remains. The highest NPP diver-sity was reached in zone HBG-B 1 where diaspores of species that pre-fer very wet conditions and the sum curve light demanding speciesindicate the prevalence of constant and very high water levels (gen-erally supporting preservation of fossils) and an open alder carr can-opy (Figs. 2 and 3). Vegetation and site conditions were most likelysimilar to those of the recent Hottonia palustris–Alnetum glutinosae(Clausnitzer, 2004). The local presence of Alnus glutinosa and/or ofdecaying wood at the peatland surface in zone HBG-B is indicatedby several NPPs, e.g. EMA-3, EMA-7, EMA-8, EMA-9, EMA-24,EMA-36, EMA-64 and EMA-134. The occurrence of grasses and sedgesis reflected by HDV-126, EMA-39, EMA-91, EMA-131 and EMA-132.

3.3.10. Prolonged sedge fen phase (HBG-C: 255–195 cm) and short-termalder carr declines (HBG 440, 330, 90 cm)

In their surface sample study, Prager et al. (2012–this issue) identifya indicator group of open fen vegetation (reed and sedge) consisting ofsome pigmented, thick walled and/or septate spores as well as tissueremains of fungi and plants, accompanied by NPPs of unknown origin.Surprisingly, most of these were not detected in the fen peat samplesof core HBG. This might be basically caused by the low number anddiversity of open fen sites in the surface sample study.

The absence of recent open fen indicators EMA-92 (possiblyfungal seta or plant hair, Prager et al. 2012–this issue), EMA-94(possibly fragment of fungal fruit-body), EMA-95 (fungal tissue)and EMA-98 (fungal fruiting body) in fossil samples might beexplained by their decay during peat development. Several NPPtypes related to alder and alder carr only occurred over ashort-time and in sedge fen phases. They most likely derived asextralocal spore rain from nearby alder stands (Fig. 4 see below).The fact that samples of the long-lasting sedge fen phase HBG-Cwere plotted in the DCA within the samples in alder carr phaseHBG-B illustrates that NPP types not always allow to differentiatebetween sedge fen and alder carr (Fig. 3A).

Sedge fen vegetation of core HBG was only reflected by a few NPPtypes related to Cyperaceae taxa that, however, also occur in aldercarrs. Compared to alder carrs the vegetation and site conditions invery wet sedge fens are rather uniform and distinct microhabitatsare rare. Furthermore water levels do not drop to the same extentduring summer months. As a result, plant remains (particularlyroots and stem bases) and the peat surface remain predominantlyunder anaerobic conditions, which strongly impede fungal metabo-lism (e.g. Williams and Crawford, 1983; Medeiros et al., 2009) and

30 A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

may result in a lower diversity of fungal spores in peat of very wetsedge fens (cf. the absence of fungal NPPs in the lake phase reflectedby zone HBG-A).

Plate

3.3.11. Alder carr phase HBG-D (195–40 cm)The local presence of alder carr in zone HBG-D is supported by the

high abundance and regular occurrence of the alder carr indicators

I.

31A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

EMA-7, EMA-8 and EMA-9 (Fig. 2). Low water levels can be inferredfrom the scarcity of above ground plant remains and of diaspores ofspecies that prefer very wet conditions (Figs. 2 and 3). Strong decom-position is reflected by a sharp increase of decaying wood remnantsEMA-7, EMA-8, EMA-9, EMA-15, EMA-62, EMA-140 and HDV-114,whereas EMA-16 (hardwood periderm) is conspicuously rarer thanin HBG-B (except for the local alder decline of HBG-90 cm, Fig. 2).Also HDV-225, EMA-132 (epidermis of Cyperaceae) and EMA-56(conidia of Alysidium resinae) occur regularly in zone HBG-D. The lat-ter seems also to be related to strong decomposition (Barthelmes etal., 2006).

Samples HBG 280 to 260 cm and HBG 100 cm of zone HBG-B 2have an intermediate degree of decomposition (POLLEN INDET. of 2–6%,Table 2). The subsequent very wet sedge fen phases of HBG-C wereprobably proceeded by rising water levels in the alder carr, whichresulted in an improved preservation of alder carr indicators andspores of wood decomposing fungi, like EMA-24, EMA-80, EMA-133,HDV-124 and HDV-143 (Figs. 2 and 3).

3.3.12. The reflection of alder carrs by NPPs: general commentsAnalysis of NPPs in other wood peat sections confirmed their use-

fulness for reconstructing vegetation, water level, canopy cover andmicrohabitats (Barthelmes, 2009). NPPs deriving from fungi andwood tissue proved to be of particular value. Fungi occur in largequantities in alder carrs, especially on decaying wood, litter, and liv-ing trees (Michael and Henning, 1967; Ellis and Ellis, 1997). Aldercarrs exhibit wide gradients of abiotic site conditions, includingwater level, pH and trophy, because of their pronounced hummock–hollow patterning (Wiebe, 1998; Jeník and Větvička, 2002). Input ofsubstantial amounts of nitrogen by Frankia-bacteria enhances decom-position and nutrient turnover with large amounts of dead plant ma-terial lying at the peatland surface. Fungal growth, decomposition oforganic matter and host plant infection are strongly facilitatedunder such conditions (Strengbom et al., 2005; Thormann, 2006;Wiedermann et al., 2007).

3.3.13. Vegetation patterns, dispersal and abundance of NPPsSome NPP types attributed to alder vegetation occur continuously

(Fig. 2) with values of 25 to 60% (Fig. 4) also during supposed openvegetation phases. The NPP types in question are predominantlysmall fungal spores and wood tissue remains of about 10–15(20)μm length and diameters of 3–8 μm (e.g. EMA-3, EMA-7, EMA-24,EMA-36, EMA-64, and EMA-134; Fig. 2) and wood tissues with aplane shape (e.g. EMA-9 and EMA-16). Considering their small size,high values of these NPPs in a probably open environment may pri-marily be related to airborne dispersal from nearby alder stands.Today, the Endinger Bruch is a mosaic of peatland forests and openvegetation patches. A similar pattern may have existed also in thepast, so that airborne NPPs may have arrived from distance of a fewhundred metres. In the fossil record of the much smaller “RodderForst” (core ROD; see Barthelmes, 2009) almost all NPP types indica-tive of alder carr strongly decrease or disappear during sedge fenphases that probably covered at least the northern part of thepeatland completely (black dots in Fig. 5). Janssen (1973) introduced

Plate I. NPPs from core HBG; bar is 10 μm. For morphological description and ecological inforMelanconis alni; 7, 8 (EMA-7, EMA-8) remnants of highly decayed wood; 9 (EMA-9), highlyconidium of cf. Excipularia fusispora; 15 (EMA-15), fragment of perforation plate in vessels ofremnant of litter decaying fungus; 27 (EMA-27A), unknown fungal spore; 38 (EMA-38), conPhaeosphaeria sp.; 44 (EMA-44), unknown origin, resemble conidia produced by e.g. Ssclerenchymatic fibre of decomposed wood; 64 (EMA-64), ascospore, probably of Sphaeriacascospore of Ceriophora palustris; 80 (EMA-80), resembles spores of Brachysporiella setosa; 8EMA-131 still attached to rootlet; 132 (EMA-132), epidermis of Cyperaceae; 133 (EMA-133)Sporormia, Sporormiella or Gliomastix murorum; 135 (EMA-135), ascospore of cf. Valsaria foedNymphaeaceae; 140 (EMA-140), corroded HDV-114.

a nowadays widely used and tested model of pollen dispersal (local,extralocal and regional pollen rain). Studies of fungal spore dispersaldynamics revealed comparable results with respect to dispersal rangeand sedimentation velocity (e.g. applicability of Stoke's Law; Tesmerand Schnittler, 2007). Compiling dozens of studies, Malloch andBlackwell (1992) concluded that the by far largest proportion of fun-gal spores usually will not escape the source plant community wherethey are produced (see also Nordén and Larsson, 2000). Also Mulderand Janssen (1999), van Geel et al. (2003) and van Geel and Aptroot(2006) concluded that most fossil fungal spores are of local origin.Our study makes plausible that an extralocal origin of (at least)small and plane NPPs has to be considered.

The abundance of EMA-3 (Melanconis alni), EMA-24 (genusHypoxylon) or EMA-64 (family Sphaeriaceae) appears to changewith a factor 3 to 10 (Fig. 5) between phases with Alnus glutinosacarr and those with sedge vegetation. Similar values were calculat-ed for EMA-133 (ascospore of cf. Sphaeriaceae, Fig. 5). Changes inthe abundance of HDV-126, HDV-112 and HDV-143 with vegetationchange were less pronounced for the first and ambiguous for thelatter (Fig. 5). Ellis and Ellis (1997) mention Carex acutiformis, C.riparia and C. elata as host plant of Clasterosporium caricinum(source of HDV-126). All these species occur recently both in aldercarrs and sedge fens (Berg et al., 2004). Van Geel and Aptroot(2006) mention Thelypteris palustris, a species that also occursboth in alder carrs and sedge fens (Berg et al., 2004), as host plantfor Diporotheca rhizophila (source of HDV-143). This might explainthe limited correlation of HDV-126 and HDV-143 with vegetationchanges.

Wood tissue NPPs (EMA-7, -8, -9 and -16) exhibit larger changesin abundance amplitudes between forest and sedge fen phases, prob-ably because of different amounts of wood in the peat. Low percent-ages and minor fluctuations could reflect extralocal or even regionalinput of the NPP types concerned (zone HBG-C, Fig. 2).

3.3.14. Non-pollen palynomorph record and peat decompositionThe number of NPP types in alder carr phases differs conspicuous-

ly per sample from up to 50 in subzone HBG-B1 to 10–20 in zoneHBG-D (Fig. 4) and is negatively correlated with POLLEN INDET. (usedas proxy for the degree of decomposition; Fig. 6). In the DCA amongother alder carr indicators EMA-27, EMA-32, EMA-36, and EMA-134,but also EMA-39 (indicative for grass-like plants), EMA-68 (indicatorfor cormophytes) and EMA-91 (indicator of very wet open vegeta-tion, Prager et al., 2012–this issue) have a high positive score onaxis 2 (top, Fig. 3B). These NPP types were found in surface sampleson sites with a wide range of water levels, but in the fossil recordthey are concentrated in better preserved peat sections with POLLEN

INDET. values of 0–4% (NPP-groups 2 and 3 of Table 2), which probablyoriginated under very wet conditions (subzone HBG-B, Fig. 2; Prageret al., 2012–this issue). These NPP types are possibly highly suscepti-ble to corrosion in phases with low or strongly fluctuating waterlevels. Fungal NPP types found in peat samples are usually clearlydominated by thick-walled, pigmented (melanised) and/or septatedspores (Plate I). These features increase resistance against decompo-sition, whereas other Alnus-associated fungi with hyaline and delicate

mation see above and Barthelmes (2009). 3 (EMA-3), conidium ofMelanconium state ofdecayed hardwood periderm; 24 (EMA-24), ascospore of cf. Hypoxylon; 36 (EMA-36),hardwood; 16 (EMA-16), hardwood periderm; 52 (EMA-52), unknown origin, possiblyidium of cf. Excipularia fusispora (Berk. et Broome) Sacc.; 39 (EMA-39), cf. ascospore ofpegazzinia; 56 (EMA-56), conidium of cf. Alysidium resinae; 62 (EMA-62), possiblyeae; 68 (EMA-68), fragment of spiralic tracheid of Cormophyta; 91 (EMA-91), possibly5 (EMA-85), cf. fungal spore; 131.a (EMA-131), basal cells of Cyperaceae rootlets, 131.b, ascospore of cf. Sphaeriaceae; 134 (EMA-134), fungal spore, might represent spores ofans; 136 (EMA-136), probably part of Nymphaeaceae; 137 (EMA-137), probably part of

Table 2NPP record in relation to decomposition degree. Alder carr samples were grouped to their POLLEN INDET. values (fig. 2) in four decomposition groups: 0–2%: HBG 440, 430, 410, 390,380, and 370 cm; 2–4%: HBG 420, 400, 340, 320, 302, 280, 270, 260, 170, 120, and 70 cm; 4–6%: HBG 310, 200, 190, 160, 151, and 80 cm; 6–9%: HBG 290, 180, 140, 130, 120, 60, 50,and 40 cm. Within these groups average values for NPPs were calculated.

POLLEN INDET. per sample (% of pollen sum) 0–2 2–4 4–6 6–9

Group Non-pollen palynomorphs % of pollen sum (Ø of samples)

1 HDV-146 (Gleotrichia type) 36.1HDV-424 (Spongillidae spicules) 0.6

2 EMA-27A (unknown fungal spore) 9.1 5.6EMA-32 (unknown fungal spore) 7.1 2.2EMA-44 (cf. conidia of Spegazzinia) 3.6 4.8EMA-85 (fungal spore) 2.7 2.7EMA-134 (fungal spore) 29.7 7.8HDV-127 (basal cells of hairs of Nymphaeaceae) 0.6 1.0HDV-137 (leaf spines of Ceratophyllum) 5.7 1.0

3 EMA-3 (conidium of Melanconis alni) 22.0 15.4 8.6EMA-16 (hardwood periderm of trees) 5.9 13.0 5.6EMA-36 (cf. conidium of Excipularia fusispora) 11.6 9.0 1.4EMA-39 (cf. ascospore of Phaeosphaeria) 15.0 4.3 2.7EMA-59 (fungal spore, resembles thalloconidia of Sporoshisma) 1.4 3.0 1.4EMA-80 (resembles spores of Brachysporiella setosa) 10.2 6.4 8.1EMA-91 (cf. ascospore of Ceriophora palustris) 12.1 1.3 4.1EMA-136 (cf. part of Nymphaeaceae) 3.3 1.7 2.7HDV-124 (ascospore of cf. Persiciospora) 4.8 4.3 8.1HDV-126 (hyphopodium of Clasterosporium caricinum) 18.5 19.0 10.1

4 EMA-64 (ascospore of cf. Sphaeriaceae) 28.4 21.4 7.2HDV-143 (spore of Diporotheca rhizophila) 21.9 21.8 7.4 2.7EMA-132 (epidermis of Cyperaceae) 5.5 33.3 18.7 2.9EMA-68 (cf. fragment of spiralic tracheid of Cormophyta) 115.3 39.7 7.7 3.2EMA-24 (ascospore of cf. Hypoxylon) 19.9 37.1 71.7 5.4EMA-131 (basal cells of Cyperaceae rootlets) 71.7 1085.0 195.4 3.5EMA-8 (remnant of highly corroded wood) 17.3 25.3 47.7 9.0EMA-133 (ascospore of cf. Sphaeriaceae) 60.9 79.2 3.0

5 EMA-1 (tracheid or tracheid fragment of vascular bundles) 59.6 535.4 1787.1 1022.2EMA-7 (remnant of highly corroded wood) 1939.5 3017.3 4137.2 2630.4EMA-9 (highly decayed hardwood periderm) 102.5 192.8 284.1 140.8EMA-57 (pyrite) 55.8 85.0 176.1 289.9EMA-62 (possibly sclerenchymatic fibre of decomposed wood) 281.4 1364.6 1545.7 2692.1EMA-15 (fragment of perforation plate of vessels in hardwood) 57.9 608.2 662.7 2102.3EMA-138 (marcasite) 106.0 150.2 311.5 799.8HDV-114 (scalariform perforation plate of vessels of Alnus, Betula, Corylus) 11.1 256.8 349.0 1163.4

6 EMA-5 (unknown origin) 0.9 6.39 6.8 9.0EMA-56 (conidium of Alysidium resinae) 1.36 8.52 11.5 19.1HDV-225 (unidentified globose microfossil) 4.64 11.15 50.2 50.9EMA-135 (ascospore of cf. Valsaria foedans) 14.62 2.7 3.9EMA-140 (corroded HDV-114) 28.19 19.0 138.5

32 A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

spores, or fungi occurring as hyphae only (e.g. ectomycorrhizal spe-cies of the genera Russula, Lactarius, Alnirhiza; Pritsch et al., 1997)may also have been present in the past, but were not preserved.

NPP types with a clear negative scoring on axis 2, including woodtissue remains HDV-114 (scalariform perforation pate), EMA-15 andEMA-140 (both decomposition remains of HDV-114; Fig. 3B) stronglyincrease in higher decomposed peat with POLLEN INDET. values of 6–9%(Table 2). Overall, the number of NPPs is however lower in samplesfrom strongly decomposed peat (HBG-D and of sample HBG290 cm). They contain predominantly decomposition residues ofwood, like EMA-7, EMA-8, EMA-9, EMA-15, EMA‐62, EMA-140 andHDV-114 (Fig. 2; NPP-groups 5 and 6 of Table 2). Only fungal sporesattributed to Alysidium resinae (EMA-56) occurred regularly.

Also the abundance of EMA-131 and EMA-132 (tissue remnants ofCyperaceae, esp. rootlets) is largely determined by the degree of peatdecomposition. Both occur with low abundances in well and poorlypreserved peat layers (POLLEN INDET. b2% and 6–9%, respectively,Table 2) but are abundant in intermediately decomposed peat(POLLEN INDET. 2–6%; Table 2). It appears that they have not yet devel-oped in well preserved peat (where Cyperaceae rootlets remain com-plete), are then abundant at an intermediate level of decomposition(where they develop from degrading rootlets) and are finallydecomposed themselves in highly degraded peat. The presence ofEMA-131 and EMA-132 thus not necessarily points at high abundanceof sedges in the fossil vegetation, but at a specific degree of

decomposition, which illustrates the importance of peat decomposi-tion for the NPP record. In general, NPPs of groups 3 and 4, which in-clude several fungal spores, seem to be more resistant todecomposition than NPPs of group 2 (Table 2).

The abundance of EMA-5, EMA-15, EMA-56, EMA-57, EMA-62,EMA-138, EMA-140 and HDV-114 is correlated to the degree of de-composition (NPP-groups 5 and 6 of Table 2), which makes themclear indicators of (high) decomposition.

4. Conclusions

The analysis of non-pollen palynomorphs of core HBG confirms theusefulness that the new EMAs from surface samples have for thepalaeoecological interpretation of wood peat deposits. The surfacesamples provided valuable information on the ecological indicatorvalue of NPPs. This value can further be tested against fossilpalaeoecological information on past vegetation and site conditionsthat pollen andmacrofossils provide. The reconstruction of vegetationand site conditions at site HBG was greatly improved by the use NPPs,especially with respect to the reconstruction of alder carrs. NPPs fur-thermore allowed to separate the lake phase clearly from the subse-quent peatland phases. Alder carrs with differences in water regimeand decomposition intensity could be distinguished by the presenceand abundance of several indicative NPP types. Due to the extralocaldispersal of alder carr related NPPs and the insufficient availability of

Fig. 4. A: Number of non-pollen palynomorph types per microfossil sample in core HBG; B: sum of diaspore types deriving from species that prefer very wet conditions (sum persample). These include Alisma plantago-aquatica, Carex appropinquata/paniculata, C. elata, C. elongata, C. pseudocyperus, C. riparia, Ceratophyllum, Cicuta virosa, Eleocharis, Hippurisvulgaris, Hydrocharis morsus-ranae, Lemna, Menyanthes trifoliata, Nymphaea, Oenanthe aquatica, Peucedanum palustre, Potamogeton, Ranunculus flammula, R. lingua, Rumexhydrolapathum, Typha latifolia, and Utricularia (Ellenberg et al., 1992; moisture values ≥9). “x”: no diaspores deriving from species that prefer very wet conditions in macrofossilsample.For detailed fossil record see Barthelmes (2009).

33A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

positive indicators for sedge fen vegetation, a clear separationbetween non-forested and forested vegetation was only possible byincluding information from themacrofossil and pollen record. Decom-position intensity appeared to affect the occurrence and abundance ofNPPs as well as the size and shape of some NPP types strongly. Planttissue remains are especially subject to alteration, which may resultin a relocation of fragmented plant tissue from the macrofossil to themicrofossil record. Only then the fragments become discernablein the palynological samples. This taphonomical process has to betaken into account when interpreting the presence of taxa. In contrastto sedge fens the abundance of phytopathogenic fungi in alder carrsprobably depends more on the nitrogen rich conditions of alder carrsrather than on the sole presence of potential host plants.

In general, NPPs are most productively studied in a broaderpalaeoecological context that includes pollen and macrofossil analysis.Thorough knowledge of mycology is necessary to minimise inconsis-tencies in interpreting fossil fungal data. This will allow the reconstruc-tion of a more complete picture of local environmental development.

4.1. Compendium of non-pollen palynomorphs (NPPS) of core HBG

Essential NPPs of the paper are presented shortly (already pub-lished HDVs and EMAs) or in detail (new EMAs). The new NPPswith identification coding of ‘EMA’ represent morphologically homo-geneous categories of microfossils (van Geel et al., 1980/81; Joostenand de Klerk, 2002), originating from peat samples of the HBG profile.Provided are morphological details (new EMAs) and information oninferred taxa, recent ecology of these taxa and/or taphonomical assump-tions (e.g. decomposition resistance or susceptibility of NPPs). Indicatorvalues and recent prevalence of NPPs derive (if not marked elsewise)from surface sample studies of Prager et al. (2012–this issue).

EMA-1: Tracheid or tracheid-fragments of vascular bundles(Prager et al., 2006).

EMA-2: Conidiophore of cf. Taeniolella alta (Ehrenberg).Taeniolella species are known as plant-associated fungi (Ellis,1971, 1976) but also live as soil fungi in the rhizosphere(Watanabe, 1992; Prager et al., 2006).EMA-3 (Plate I.1): Conidium of the Melanconium state ofMelanconis alni Tul and C. Tul (Prager et al., 2006). Melanconisalni is a fungus common on living and dead twigs and leaves ofAlnus glutinosa (Sieber et al., 1991; Ellis and Ellis, 1997). EMA-3 re-cently indicates presence of alder and occurred in core HBG pre-dominantly in alder carrs. Can be of extralocal origin (see above).EMA-4: Fungal spore (Prager et al., 2006). Possibly immature stateof EMA-3. EMA-4 recently indicates presence of alder, occurred fossilpredominantly in alder carrs. Can be of extralocal origin (see above).EMA-7 (Plate I.2): Possibly remnant of highly decayed wood(Prager et al., 2006). EMA-7 originates from hardwood periderm(EMA-16; Barthelmes, 2009). High abundances indicate recentlythe presence of trees (alder, birch?). In core HBG high valueswere restricted to alder carr samples. Low values can also be ofextralocal origin.EMA-8 (Plate I.3): Possibly remnant of highly decayed wood(Prager et al., 2006). EMA-8 indicates presence of trees (alder,birch?). In core HBG high values occurred in alder carr samples.Low values can also be of extralocal origin.EMA-9 (Plate I.4): Highly decayed hardwood periderm (Prager etal., 2006). EMA-9 recently indicates presence of alder. In core HBGhigh values occurred in alder carr samples. Low values can also beof extralocal origin.EMA-13: Fungal spore, probably of smut fungus (Barthelmes et al.,2006).EMA-15 (Plate I.7): Fragment of perforation plate in vessels ofhardwood, e.g. Alnus, Betula or Corylus (Prager et al., 2006).EMA-15 and HDV-114 recently indicate presence of alder and/orbirch. In core HBG high values are restricted to alder carr samplesand indicate heavy decomposition.

Fig. 5. Behaviour of alder carr indicating NPP types of core HBG at transitions between alder carr and sedge fen (regarding first and last samples of [sub]zones, fig. 2). Only NPPs thatoccurred over more than three (sub)zone borders were used. Median is calculated if data on particular NPP types were available from both, core HBG and core ROD. Black columns:abundance shift of alder carr indicators contradicts expectations (increase from alder carr to sedge fen and decrease from sedge fen to alder carr, respectively). To enable factorcalculation “1” is added if NPP percentage was zero at one site of zone border.

Fig. 6. Diagram shows the correlation between POLLEN INDET. (fig. 2) and the sum of NPPtaxa per sample (fig. 4). Established alder carr samples only (without sedge fen and lakesamples HBG 90–112 cm, 210–250 cm, 440–500 cm and HBG 330 cm, Barthelmes,2009).

34 A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

EMA-16 (Plate I.8): Hardwood periderm of trees, e.g. Alnus,Betula, Salix (Barthelmes et al., 2006). In core HBG high valuesoccurred in alder carr samples. Low values can also be ofextralocal origin.EMA-24 (Plate I.5): Ascospore of cf. Hypoxylon (Prager et al.,2006). This genus comprises wood-decomposing and endophyticspecies (Tang et al., 2009; Unterseher and Schnittler, 2010). Onlyslightly different morphology as EMA-64; it might be reasonableto merge these types to one morphotype. Might also includespores of fungal genus Rosellinia (IBB-31, Montoya et al., 2010),which however, also often grow on wood and bark (Ellis andEllis, 1997). See also Type UG-1329 of Gelorini et al. (2011) andTM-347 of Cugny (2011). EMA-24 is recently possibly an indicatorfor the presence of alder, though a variety of other host associa-tions exists. In core HBG high values occurred in alder carr sam-ples. Low values can also be of extralocal origin.EMA-27A (Plate I.10): Unknown fungal spore. EMA-27A (EMA-27,Prager et al., 2006) is recently an indicator for above ground alderremnants and thus for on site presence of alder. In core HBG it isnearly restricted to samples from very wet alder carr and thusprobably susceptible to corrosion.EMA-32: Unknown fungal spore (Prager et al., 2006). Indicates re-cent the presence of alder. In core HBG it is nearly restricted tosamples from very wet alder carr and thus probably susceptibleto corrosion.EMA-36 (Plate I.6): First described by Prager et al. (2006); nowidentified as conidium of Excipularia fusispora (Berk. et Broome)Sacc. by Prager et al. (2012–this issue). E. fusispora is commonon decayed wood and bark of deciduous trees (e.g. Alnus, Populus,Salix; Yurchenko, 2001). See also TM-037C2 of Cugny (2011).EMA-36 is recently indicative for the presence of alder. In core

HBG it is nearly restricted to samples from very wet alder carrand thus probably susceptible to corrosion. Low values can alsobe of extralocal origin.EMA-38 (Plate I.11): First described by Prager et al. (2006), nowidentified as conidium of cf. Excipularia fusispora (Berk. et Broome)Sacc. by Prager et al. (2012–this issue). E. fusispora is common ondecaying wood and bark of deciduous trees (e.g. Alnus, Populus,Salix; Yurchenko, 2001) and recent indicative for the presence ofalder. EMA-36 and EMA-38 are different morphological types,but conidia of the same species. See also Type UG-1147 ofGelorini et al. (2011).

35A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

EMA-39 (Plate I.12): First described by Prager et al. (2006), nowidentified as cf. ascospore of Phaeosphaeria sp. by Prager et al.(2012–this issue). Phaeosphaeria species are serious pathogens ofcereals, grasses, sedges, rushes and other grass-like plants(Shoemaker and Babcock, 1989). EMA-39 is recently possibly in-dicative for the presence of sedges and grasses in forested aswell as open fen vegetation. In core HBG it only occurred in sam-ples of very wet alder carrs. The abundance of phytopathogenicfungi (e.g. EMA-39) in alder carrs probably depends on the nitro-gen rich conditions of alder carrs (see above). EMA-39 probably issusceptible to corrosion.EMA-44 (Plate I.13): Unknownorigin (Prager et al., 2006). Resemblesconidia produced by Spegazzinia (Ellis, 1976). Similar to HDV-1018(van Geel et al., 2011), also attributed to Spegazzinia, but HDV-1018is almost twice as large as EMA-44. Occurs recently in alder carrswith different water levels, but also in one open sedge fen (AnjaPrager, pers. comm.). In core HBG high values are restricted to aldercarr samples. Low values can also be of extralocal origin.EMA-52 (Plate I.9): Possibly no algal remain (Prager et al., 2006),but rather remnant of litter decaying fungus. Recently indicativefor above ground remnants and thus presence of alder.EMA-56 (Plate I.14): Conidium of Alysidium resinae (Fr.) M.B. Ellis(Barthelmes et al., 2006), an anamorph of the corticioid, wooddecaying basidiomycete genus Botryobasidium (Ellis and Ellis,1997). In recent fen vegetation only found in birch carr and verywet alder carr (Anja Prager, pers. comm.). In core HBG predomi-nantly occurring in highly decayed wood peat samples of zoneHBG-D (points at strong decomposition and low or fluctuatingwater levels).EMA-59: Fungal spore or conidiophore fragment (Prager et al.,2012–this issue); resembles thalloconidia of Sporoschisma species,but also the conidiophores (or their fragments) of Arthriniumspecies (Ellis and Ellis, 1997). Might recently indicate alder carrvegetation. In core HBG high values restricted to alder carr samples.Low values can be of extralocal origin.EMA-62 (Plate I.15): Wooden remain, cf. sclerenchymatic fibres,elongated, (15)30–60(210)×(4)6–12(20) μm, bright yellow tobrown and psilate. When less corroded, with shape of a com-pressed cylinder with at least one incline cut end, strongly corrod-ed with irregular shape and small hollows and bubbles beneaththe surface caused by fungal decay. Occurred in birch dead woodsamples from recent birch and alder carrs (Anja Prager, pers.comm.). In core HBG high values restricted to alder carr sampleswith focus on strongly decayed wood peat samples of zoneHBG-D. Low values can be of extralocal origin.EMA-64 (Plate I.16): Bean-shaped (dorsally curved, ventrally al-most straight), 12–15×5 μm, sometimes with germ slit, mid todark brown, psilate. Ascospore, probably of Sphaeriaceae,(Barthelmes, 2009), a family of mostly wood decomposing fungi(Breitenbach and Kränzlin, 1981). Only slightly different morphol-ogy as EMA-24; it might be reasonable to merge these types to onemorphotype. Might also include spores of fungal genus Rosellinia(IBB-31, Montoya et al., 2010), which however, also often growon wood and bark (Ellis and Ellis, 1997). See also Type UG-1329of Gelorini et al. (2011) and TM-347 of Cugny (2011). Occurs re-cently in alder carrs with different water levels (Anja Prager,pers. comm.). In core HBG high values restricted to alder carr sam-ples. Low values can be of extralocal origin.EMA-68 (Plate I.17): Possibly fragment of spiralic tracheid(Cormophyta; Prager et al., 2012–this issue), known from roots ofe.g. Cyperaceae. The type is recently produced in alder carrs andsedge fens of differentwater levels, but is in core HBG predominant-ly preserved in peat that accumulated under very wet conditions.EMA-68 is probably susceptible to corrosion.EMA-80 (Plate I.19): Fungal spore, ovoid, mostly 2-septate (rarely1-septate), spore consists of one large apical cell (17–23 μm),

middle brown and two (rarely one) small proximal cells (3–6 μm), hyaline to very pale brown, constricted at septa, pore inmost apical septum, whole spore 25–32×11–17 μm, sporecompletely psilate, but wall seems to be slightly undulating. Re-sembles spores of Brachysporiella setosa (Berk. and Curt.) M.B.Ellis comb. nov., a fungus occurring on decayed wood in “moist”places (Ellis, 1959). See also TM-371B of Cugny (2011).EMA-85 (Plate I.20): cf. fungal spore (or fragment of it), cylindricelongated with rounded ends, sometimes slightly curved, 33–122×7–12 μm, muriform with transversal and longitudinal septagiving an irregular pattern, single cells angular and 5–6×5–10 μm, middle to light brown and psilate. Occurs recently inopen fen vegetation with different water levels and somewhatdrier alder carrs (Anja Prager, pers. comm.). In core HBG largelyrestricted to very wet conditions in alder carr and sedge fen.EMA-91 (Plate I.18): Possibly ascospore of Ceriophora palustris(Berk. and Broome) Höhn (Prager et al., 2012–this issue), a funguson Carex (Ellis and Ellis, 1997). Recently possibly indicative ofopen vegetation. Also occurring in core HBG in samples fromvery wet alder carr.EMA-131 (Plate I.21): Single cells (10–13×7–11 μm) rectangular,contact point with rootlet somewhat widened, yellow to hyaline.Mostly single cells, sometimes in groups or attached to rootlets.Basal cells of Cyperaceae rootlets, partly still attached to rootlet(Plate I.26). High abundances indicate local presence ofCyperaceae, possibly sedges and enhanced decomposition ofCyperaceae rootlets. Decline of this type can be caused by im-proved fossil preservation (inhibiting decomposition ofCyperaceae rootlets) or decreasing cover of Cyperaceae at the site.EMA-132 (Plate I.22): Yellow to hyaline tissue fragments of differ-ent size. Single cells small, elongated (5–10×longer than wide)and regularly and finely undulated. Probably epidermis ofCyperaceae. High abundances indicate local presence ofCyperaceae, possibly sedges, but may be enhanced by lowerwater levels and resulting increased oxidative decomposition oflarger Cyperaceae tissue. Decline of this type can be caused by im-proved fossil preservation (inhibiting decomposition ofCyperaceae tissue), declined fossil preservation (decompositioneven of Cyperaceae tissue fragments) or decreasing cover ofCyperaceae at the site.EMA-133 (Plate I.23): Bean shaped to ellipsoid and somewhat flat-tened, 16–18 μm×8–11 μm, with longitudinal furrow of 8–9 μmlength, brown, psilate. Ascospore of cf. Sphaeriaceae, a familywhich includes genera of wood-decomposing fungi (Breitenbachand Kränzlin, 1981).EMA-134 (Plate I.24): Fungal spore (Prager et al., 2012–this issue),might represent spores of the coprophilous and endophytic generaSporormia, Sporormiella or Gliomastix (Ahmed and Cain, 1972) orbelongs to the cosmopolitan fungal genus Torula which includesspecies on litter, soil and dung (Seiffert et al., 2011). Occurs recent-ly in alder carr and open fen vegetation. EMA-134 was recentlyfound with high values in rather dry alder carrs, but is predomi-nantly preserved in peat of very wet alder carrs (core HBG). Prob-ably EMA-134 is strongly susceptible to corrosion.EMA-135 (Plate I.25): 12–14×5–6 μm, bean-shaped, one-septate,septum with pore, brown, psilate. Ascospore of cf. Valsaria foedans(P. Karsten) Sacc., a fungus occurring on dead branches of e.g.Alnus, Betula and Castanea (Ellis and Ellis, 1997). See alsoTM-307 of Cugny (2011).EMA-136 (Plate I.28): Hyaline tissue, distinctively folded, 90–130×15–50 μm, psilate. Probably part of Nymphaeaceae, becausesometimes attached to HDV-127.EMA-137 (Plate I.27): Compact yellow to light brown tissue withrectangular to trapezoid cells, single cells 19–30×52–80 μm, frag-ments 30–90×20–50 μm. Probably part of Nymphaeaceae, be-cause sometimes attached to HDV-127.

36 A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

EMA-140 (Plate I.29): Fragments of different size (mainly 40–100×20–40 μm), yellowish-hyaline. Corroded HDV-114 (seebelow). EMA-140 indicates heavy decomposition – even of wood –

implying low or strongly fluctuating water levels.HDV-112: First description by Bakker and van Smeerdijk (1982);identified as ascospore of Cercophora by van Geel and Aptroot(2006). This genus comprises species of coprophilous fungiwhich also occur on decaying wood, culms, stems and leaves(Ellis and Ellis, 1997). Occurs recently in open fen vegetation,alder and birch carrs with different water levels. In core HBGhigh values in alder carr zones which emphasises its affinity todecaying wood.HDV-114: Scalariform perforation plate, occurring in vessels ofBetula, Alnus, Corylus and Myrica (Pals et al., 1980; related toEMA-15). Indicative for recent birch and alder carrs. In core HBGwith high abundances in strongly decomposed zone HBG-D.Points at heavy decomposition – even of wood – which implieslow or strongly fluctuating water levels.HDV-126: First description by Pals et al. (1980); identified ashyphopodium of Clasterosporium caricinum by van Geel andAptroot (2006). Occurs recently in open fen vegetation and lessabundantly in somewhat drier alder carrs (Anja Prager, pers.comm.). The abundance of phytopathogenic fungi (e.g. HDV-126)in alder carrs probably depends on the nitrogen rich conditionsof alder carrs (see above).

Acknowledgements

The palynological research of core HBG was financed by the Feder-al State of Mecklenburg-Western Pomerania (project EMAU 13-[95,96] 1997 ‘Pollen und Großrestanalytik’) and supervised by K. Billwitz.H. Rabe prepared the pollen samples. The analysis of macrofossils andnon-pollen palynomorphs was supported by the DeutscheBundesstiftung Umwelt (DBU) within the context of theALNUS-project of Greifswald University. 14C-AMS dating was carriedout by the Poznań Radiocarbon Laboratory headed by T. Goslar.

References

Ahmed, S.I., Cain, R.F., 1972. Revision of the genera Sporormia and Sporormiella. Canadi-an Journal of Botany 50, 419–477.

Akkermans, A.D.L., van Dijk, C., 1981. The formation and nitrogen fixing activity of theroot nodules of Alnus glutinosa under field conditions. In: Nutman, P.E. (Ed.),Symbiotic Nitrogen Fixation in Plants. Cambridge University Press, Cambridge,pp. 511–520.

Bakker, M., van Smeerdijk, D.G., 1982. A paleoecological study of a late Holocene sec-tion from “Het Ilperveld”, Western Netherlands. Review of Palaeobotany and Paly-nology 36, 95–163.

Barthelmes, A., 2009. Vegetation dynamics and carbon sequestration of Holocene alder(Alnus glutinosa) carrs in NE Germany. PhD Thesis, Greifswald University, Greifswald.

Barthelmes, A., Prager, A., Joosten, H., 2006. Palaeoecological analysis of Alnus woodpeats with special attention to non-pollen palynomorphs. Review of Palaeobotanyand Palynology 141, 33–51.

Bauer, I.E., 2004. Modelling effects of litter quality and environment on peat accumula-tion over different time-scales. Journal of Ecology 92, 661–674.

Beijerinck, W., 1947. Zadenatlas der Nederlandse Flora [Seed Atlas of the Dutch Flora].Backhuys and Meesters, Wageningen.

Die Planzengesellschaften Mecklenburg-Vorpommerns und ihre Gefährdung. In: Berg,C., Dengler, J., Abdank, A., Isermann, M. (Eds.), Weißdorn, Jena, pp. 435–448.

Berggren, G., 1969. Atlas of Seeds and Small Fruits of Northwest-European Plant Spe-cies With Morphological Descriptions: 2 — Cyperaceae. Swedish National ScienceResearch Council, Stockholm.

Berglund, B.E., Birks, H.J.B., Ralska-Jasiewiczowa, M., Wright, H.E., 1996. PalaeoecologicalEvents During the Last 15000 years. J. Wiley, Chichester.

Binkley, D., Sollins, P., Bell, R., Myrold, D., 1992. Biogeochemistry of adjacent coniferand alder-conifer stands. Ecology 73, 2022–2033.

Blackford, J.J., Innes, J.B., 2006. Linking current environments and processes to fungalspore assemblages: surface NPM data from woodland environments. Review ofPalaeobotany and Palynology 141, 179–187.

Blackford, J.J., Innes, J.B., Hatton, J.J., Caseldine, C.J., 2006. Mid-Holocene environmentalchange at Black Ridge Brook, Dartmoor, SW England: a new appraisal based onfungal spore analysis. Review of Palaeobotany and Palynology 141, 189–201.

Bos, J.A.A., van Geel, B., Groenewoudt, B.J., Lauwerier, R.C.G.M., 2005. Early Holocene en-vironmental change, the presence and disappearance of early Mesolithic habitation

near Zutphen (The Netherlands). Vegetation History and Archaeobotany 15, 27–43.Breitenbach, J., Kränzlin, G., 1981. Pilze der Schweiz. Bd. I: Ascomyceten. Mycologia, Luzern.Brown, A.G., 1988. The palaeoecology of Alnus (alder) and the Postglacial history of

floodplain vegetation. Pollen percentage and influx data from the West Middlands,United Kingdom. New Phytologist 110, 425–436.

Clausnitzer, U., 2004. 30 Klasse: Alnetea glutinosae Br.-Bl. and Tx. ex Westhoff and al.1946 — Erlen-Eschen- und Weiden-Gehölze nährstoffreicher Feucht- und Nass-Standorte außerhalb der Stromauen. In: Berg, C., Dengler, J., Abdank, A.,Isermann, M. (Eds.), Die Planzengesellschaften Mecklenburg-Vorpommerns undihre Gefährdung. Weißdorn, Jena, pp. 435–448.

Cugny, C. 2011. Apports des microfossiles non-polliniques à ľhistoire du pastoralismesur le versant nord pyrénéen. Thèse en vue de ľ obtention du Doctorat de ľUniversité de Toulouse. 280 p. + Annex.

Cugny, C., Mazier, F., Galop, D., 2010. Modern and fossil non-pollen palynomorphs fromthe Basque mountains (western Pyrenees, France): the use of coprophilous fungi toreconstruct pastoral activity. Vegetation History and Archaeobotany 19, 391–408.

Davis, O.K., Shafer, D.S., 2005. Sporormiella fungal spores, a palynological means ofdetecting herbivore density. Palaeogeography, Palaeoclimatology, Palaeoecology237, 40–50.

Dawson, J.O., Funk, D.T., 1981. Seasonal change in foliar nitrogen concentrations ofAlnus glutinosa. Forestry Sciences 27, 239–243.

de Klerk, P., 2002. Changing vegetation patterns in the Endinger Bruch area(Vorpommern, NE Germany) during the Weichselian Lateglacial and Early Holo-cene. Review of Palaeobotany and Palynology 119, 275–309.

de Klerk, P., Janssen, C.R., Joosten, J.H.J., 1997. Patterns and processes in natural wetlandvegetation in the Dutch fluvial area: a palaeoecological study. Acta BotanicaNeerlandica 46, 147–159.

Dommain, R., Couwenberg, J., Joosten, H., 2011. Development and carbon sequestrationof tropical peat domes in south-east Asia: links to postglacial sea-level changes andHolocene climate variability. Quaternary Science Reviews 30, 999–1010.

Ejarque, A., Miras, Y., Riera, S., 2011. Pollen and non-pollen palynomorph indicators of veg-etation and highland grazing activities obtained frommodern surface and dung datasetsin the eastern Pyrenees. Review of Palaeobotany and Palynology 167, 123–139.

Ellenberg, H., Weber, H.E., Düll, R., Wirth, V., Werner, W., Paulißen, D., 1992.Zeigerwerte der Gefäßpflanzen Mitteleuropas, Ed. 2. Scripta Geobotanica, 18.Goltze KG, Göttingen.

Ellis, M.B., 1959. Clasterosporium and some allied Dematiaceae–Phragmosporae II. My-cological Papers 72, 1–75.

Ellis, M.B., 1971. Dematiaceous Hyphomycetes. Oxford University Press, Kew, England.Ellis, M.B., 1976. More Dematiacaeous Hyphomycetes. CAB International, Wallingford, UK.Ellis, M.B., Ellis, J.P., 1997. Microfungi on Land Plants — An Identification Handbook.

Richmont Publishing, Slough.Fægri, K., Iversen, J., 1989. Textbook of Pollen Analysis (Revised by Fægri, K., Kaland, P.,

E, Krzywinski, K.). John Wiley and Sons, Chichester.Feeser, I., O'Connell, M., 2010. Late Holocene land-use and vegetation dynamics in an up-

land karst region based on pollen and coprophilous fungal spore analyses: an examplefrom the Burren, western Ireland. Vegetation History and Archaeobotany 19, 409–426.

Gelorini, V., Verbeken, A., van Geel, Bas, Cocquyt, C., Verschuren, D., 2011. Modern non-pollen palynomorphs from East African lake sediments. Review of Palaeobotanyand Palynology 164, 143–173.

Graf, M.-T., Chmura, G.L., 2006. Development of modern analogues for natural, mowedand grazed grasslands using pollen assemblages and coprophilous fungi. Review ofPalaeobotany and Palynology 141, 139–149.

Grimm, E.C., 1992. TILIA 1.12 and TILIAGRAPH 1.18 (Software). Illinois State Museum,Springfield.

Grimm, E.C., 2004. TGView 2.0.2 (Software). Illinois State Museum, Springfield.Grosse-Brauckmann, G., 1972. Über pflanzliche Makrofossilien mitteleuropäischer

Torfe. I. Gewebereste krautiger Pflanzen und ihre Merkmale. Telma 2, 19–55.Grosse-Brauckmann, G., Streitz, B., 1992. Pflanzliche Makrofossilien mitteleuropäischer

Torfe. III. Früchte, Samen und einige Gewebe (Fotos von fossilen Pflanzenresten).Telma 22, 53–102.

Innes, J., Blackford, J., Simmons, I., 2010. Woodland disturbance and possible land-useregimes during the Late Mesolithic in the English uplands: pollen, charcoal andnon-pollen palynomorph evidence from Bluewath Beck, North York Moors, UK.Vegetation History and Archaeobotany 19, 439–452.

Irmler, U., 1995. Veränderungen in der Zusammensetzung der Streufauna während desAbbaus von Erlenstreus. Mitteilungen der Deutschen Bodenkundlichen Gesell-schaft 76, 623–626.

Janssen, C.R., 1959. Alnus as a disturbing factor in pollen diagrams. Acta BotanicaNeerlandica 8, 55–58.

Janssen, C.R., 1973. Local and regional pollen deposition. In: Birks, H.J.B., West, R.G.(Eds.), Quaternary Plant Ecology. : Proc. 14th Symp. of the British Ecological Soci-ety. Blackwell, Oxford, pp. 31–42.

Jeník, J., Větvička, V., 2002. Regressive development of an alder carr. In: Květ, J., Jeník, J.,Soukupová, L. (Eds.), Freshwater Wetlands and Their Sustainable Future — A CaseStudy of the Trěboň Basin Biosphere Reserve, Czech Republic: Man and the Bio-sphere, 28, pp. 283–291.

Jumpponen, A., Trappe, J.M., 1998. Dark septate endophytes: a review of facultativebiotrophic root-colonising fungi. New Phytologist 140, 295–310.

Kac, N.J., Kac, S.V., 1933. Atlas rastitel'nych ostatkow v torfe (Atlas of plant remnants inpeat). Gosudarstvennoje izdatel'stvo kolchoznoj i sovchoznoj literatury, Moskva.(in Russian).

Kac, N.J., Kac, S.V., Kipani, M.G., 1965. Atlas i opredelitel plodov i cemyanvstrechayushchukhsya v chetvertichnykh otlozheniyakh SSSR. Atlas and Keys ofFruits and Seeds Occurring in the Quaternary Deposits of USSR. Nauka, Moscow.(in Russian).

37A. Barthelmes et al. / Review of Palaeobotany and Palynology 186 (2012) 22–37

Klingensmith, K.M., Vancleve, K., 1993. Denitrification and nitrogen fixation in flood-plain successional soils along the Tanana river, Interior Alaska. Canadian Journalof Forest Research 23, 956–963.

Kramer, A., Herzschuh, U., Mischke, S., Zhang, C., 2010. Late Quaternary environmentalhistory of the south-eastern Tibetan Plateau inferred from the Lake Naleng non-pollen palynomorph record. Vegetation History and Archaeobotany 19, 453–468.

Kuhry, P., 1997. The palaeoecology of a treed bog in western boreal Canada: a studybased on microfossils, macrofossils and physio-chemical properties. Review ofPalaeobotany and Palynology 96, 183–224.

Lang, G., 1994. Quartäre Vegetationsgeschichte Europas. Fischer, Jena.Malloch, D., Blackwell, M., 1992. Dispersal of fungal diaspores, In: Carroll, G.C.,

Wicklow, D.T. (Eds.), The Fungal Community, Its Organization and Role in the Eco-system, 2nd edition. Marcel Dekker Inc., pp. 147–171.

Marek, S., 1965. Biologia i stratygrafia torfowisk olszynowych w Polsce. ZeszymyProblemowe Postepow Nauk Rolniczych 57, 5–158 (in Polish).

Medeiros, A.O., Pascoal, C., Graca, M.A.S., 2009. Diversity and activity of aquatic fungiunder low oxygen conditions. Freshwater Biology 54, 142–149.

Meusel, H., Jäger, E., Weinert, E., 1965. Vergleichende Chorologie der zentraleuropäischenFlora. Bd.1. Fischer, Jena.

Michael, E., Henning, B., 1967. Handbuch für Pilzfreunde. Bd. 4. Fischer, Jena.Mighall, T.M., Cortizas, A.M., Biester, H., Turner, S.E., 2006. Proxy climate and vegetation

changes during the last five millennia in NW Iberia: Pollen and non-pollenpalynomorph data from two ombrotrophic peat bogs in the North Western IberianPeninsula. Review of Palaeobotany and Palynology 141, 203–223.

Mingram, J., Negendank, F.W., Brauer, A., Berger, D., Hendrich, A., Köhler, M., Usinger,H., 2007. Long cores from small lakes—recovering up to 100 m-long lake sedimentsequences with a high-precision rod-operated piston corer (Usinger-corer). Jour-nal of Paleolimnology 37, 517–528.

Montoya, E., Rull, V., van Geel, B., 2010. Non-pollen palynomorphs from surface sedi-ments along an altitudinal transect of the Venezuelan Andes. Palaeogeography,Palaeoclimatology, Palaeoecology 297, 169–183.

Moore, P.D., Webb, J.A., Collinson, M.E., 1991. Pollen Analysis. Blackwell, Oxford.Mulder, C., Janssen, C.R., 1999. Occurrence of pollen and spores in relation to present-day

vegetation in a Dutch heathland area. Journal of Vegetation Science 10, 87–100.Mulder, C., Breure, A.M., Joosten, H., 2003. Fungal functional diversity inferred along

Ellenberg's abiotic gradients: palynological evidence from different soil microbiota.Grana 42, 55–64.

Nilson, Ö., Helmquist, H., 1967. Studies on the nutlet structure of South Scandinavianspecies of Carex. Botaniska Notiser 120, 460–485.

Nordén, B., Larsson, K.-H., 2000. Basidiospore dispersal in the old-growth forest fungusPhlebia centrifuga (Basidiomycetes). Nordic Journal of Botany 20, 215–219.

Odier, E., Monties, B., 1983. Absence of microbial mineralization of lignin in anaerobicenrichment cultures. Applied and Environment Microbiology 46, 661–665.

Pals, J.P., van Geel, B., Delfos, A., 1980. Palaeoecological studies in the Klokkeweel bognear Hoogkarspel (Noord Holland). Review of Palaeobotany and Palynology 30,371–418.

Pokorný, P., Klimešova, J., Klimeš, L., 2000. Late Holocene history and vegetation dy-namics of a floodplain alder carr: a case study from Eastern Bohemia, Czech Repub-lic. Folia Geobotanica 35, 43–58.

Prager, A., Barthelmes, A., Theuerkauf, M., Joosten, H., 2006. Non-pollen palynomorphsfrom modern Alder carrs and their potential for interpreting microfossil data frompeat. Review of Palaeobotany and Palynology 141, 7–31.

Prager, A., Theuerkauf, M., Couwenberg, J., Barthelmes, A., Aptroot, A., Joosten, H., 2012.NPPs of fen vegetation types with emphasis on Alder carrs - a surface sample studyfrom NE-Germany 186, 38–57 (this issue).

Pritsch, K., Munch, J.C., Buscot, F., 1997. Morphological and anatomical characterisationof black alder Alnus glutinosa (L.) Gaertn. ectomycorrhizas. Mycorrhiza 7, 201–216.

Punt, W. (Ed.), 1976. The Northwest European Pollen Flora I. Elsevier, Amsterdam.Punt, W., Blackmore, S. (Eds.), 1991. The Northwest European Pollen Flora VI. Elsevier,

Amsterdam.Punt, W., Clarke, G.C.S. (Eds.), 1984. The Northwest European Pollen Flora IV. Elsevier,

Amsterdam.Reimer, P.J., Baillie, M.G.L., Bard, E., Bayliss, A., Beck, J.W., Bertrand, C.J.H., Blackwell,

P.G., Buck, C.E., Burr, G.S., Cutler, K.B., Damon, P.E., Edwards, R.L., Fairbanks, R.G.,Friedrich, M., Guilderson, T.P., Hogg, A.G., Hugher, K.A., Kromer, B., McCormac, G.,Manning, S., Ramsey, C.B., Reimer, R.W., Remmele, S., Southon, J.R., Stuiver, M.,Talamo, S., Taylor, F.W., Van der Plicht, J., Weyhenmeyer, C.E., 2004. Intcal04 terres-trial radiocarbon age calibration, 0–26 cal kyr BP. Radiocarbon 46, 1029–1058.

Ryan, P.A., Blackford, J.J., 2010. Late Mesolithic environmental change at Black Heath,south Pennines, UK: a test of Mesolithic woodland management models using pol-len, charcoal and non-pollen palynomorph data. Vegetation History andArchaeobotany 19, 545–558.

Schaeffer, F., Schachtschabel, P., 1992. Lehrbuch der Bodenkunde, 13. Aufl., Enke,Stuttgart.

Seiffert, K., Morgan-Jones, G., Gams, W., Kendrick, B., 2011. The Genera ofHyphomycetes. CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands.

Shoemaker, R.A., Babcock, C.E., 1989. Phaeosphaeria. Canadian Journal of Botany 67,1500–1599.

Sieber, T.N., Sieber-Canavesi, F., Dorworth, C.E., 1991. Endophytic fungi of red alder(Alnus rubra) leaves and twigs in British Columbia. Canadian Journal of Botany69, 407–411.

Smol, J.P., Birks, H.J., Last, W.M. (Eds.), 2001. Tracking Environmental Change UsingLake Sediments. Vol. 3: Terrestrial, Algal and Siliceous Indicators. Kluwer AcademicPublishers, Dordrecht, Boston, London.

Strengbom, J., Englund, G., Ericson, L., 2005. Experimental scale and precipitation mod-ify effects of nitrogen addition on a plant pathogen. Journal of Ecology 94, 227–233.

Stuiver, M., Reimer, P.J., 1993. Extended 14C data base and revised Calib 3.0 14C age cal-ibration program. Radiocarbon 35, 215–230.

Stuiver, M., Reimer, P.J., 2005. CALIB Rev. 5.0.1. (software).Tang, A.M.C., Jeewon, R., Hyde, K.D., 2009. A re-evaluation of the evolutionary relation-

ships within the Xylariaceae based on ribosomal and protein-coding gene se-quences. Fungal Diversity 34, 127–155.

Telford, R.J., Heegaard, E., Birks, H.J.B., 2004. The intercept is a poor estimate of a cali-brated radiocarbon age. Holocene 14, 296–298.

Tesmer, J., Schnittler, M., 2007. Sedimentation velocity of myxomycete spores. Myco-logical Progress 6, 229–234.

Thormann, M.N., 2006. Diversity and function of fungi in peatlands: a carbon cyclingperspective. Canadian Journal of Soil Science 86, 281–293.

Unterseher, M., Schnittler, M., 2010. Species richness analysis and ITS rDNA phylogenyrevealed the majority of cultivable foliar endophytes from beech (Fagus sylvatica).Fungal Ecology 3, 366–378.

van der Wiel, A.M., 1982. A palaeoecological study of a section from the foot of thehazendonk (Zuid Holland, The Netherlands), based on the analysis of pollen,spores and macroscopic plant remains. Review of Palaeobotany and Palynology38, 35–90.

van Geel, B., 1972. Palynology of a section from the raised peat bog “WietmarscherMoor”, with special reference to fungal remains. Acta Botanica Neerlandica 21,261–284.

van Geel, B., 1978. A paleoecological study of Holocene peat bog sections in Germanyand The Netherlands, based on the analysis of pollen, spores and macro- and mi-croscopic remains of fungi, algae, cormophytes and animals. Review ofPalaeobotany and Palynology 25, 1–120.

van Geel, B., Aptroot, A., 2006. Fossil ascomycetes in Quaternary deposits. NovaHedwigia 82, 313–329.

van Geel, B., Bohncke, S.J.P., Dee, H., 1980/81. A palaeoecological study of an upper LateGlacial and Holocene sequence from “De Borchert”, The Netherlands. Review ofPalaeobotany and Palynology 31, 367–448.

van Geel, B., Hallewas, D.P., Pals, J.P., 1982/83. A Late Holocene deposit under theWestfriese Zeedijk near Enkhuizen (Prov. of N-Holland, The Netherlands):palaeoecological and archeological aspects. Review of Palaeobotany and Palynology38, 269–335.

van Geel, B., Coope, G.R., Hammen, T., 1989. Palaeoecology and stratigraphy of the LateGlacial section at Usselo (The Netherlands). Review of Palaeobotany and Palynolo-gy 60, 25–129.

van Geel, B., Buurman, J., Brinkkemper, O., Schelvis, J., Aptroot, A., van Reenen, G.,Hakbijl, T., 2003. Environmental reconstruction of a Roman Period settlementsite in Uitgeest (The Netherlands), with special reference to coprophilous fungi.Journal of Archaeological Science 30, 873–883.

van Geel, B., Gelorini, V., Lyaruu, A., Aptroot, A., Rucina, S., Marchant, R., SinningheDamsté, J.S., Verschuren, D., 2011. Diversity and ecology of tropical African fungalspores from a 25,000-year palaeoenvironmental record in southeastern Kenya. Re-view of Palaeobotany and Palynology 164, 174–190.

Waller, M.P., 1993. Flandrian vegetational history of south-eastern England. Pollen datafrom Pannel Bridge, East Sussex. New Phytologist 124, 345–369.

Waller, M.P., 1994. Flandrian vegetational history of south-eastern England. Stratigra-phy of the Brede valley and pollen data from Brede Bridge. New Phytologist 126,369–392.

Watanabe, T., 1992. Taeniolella phialosperma sp.nov. from Japan. Mycologia 84,478–483.

Wiebe, C., 1998. Ökologische Charakterisierung von Erlenbruchwäldern und ihrenEntwässerungsstadien: Vegetation und Standortverhältnisse. Mitteilungen derArbeitsgemeinschaft Geobotanik in Schleswig-Holtstein, 56. Hansa-Druck, Kiel.

Wiedermann, M.M., Nordin, A., Gunnarsson, U., Nilsson, M.B., Ericson, L., 2007. Globalchange shifts vegetation and plant–parasite interactions in a boreal mire. Ecology88, 454–464.

Williams, R.T., Crawford, R.L., 1983. Microbial diversity of Minnesota peatlands. Micro-bial Ecology 9, 201–214.

Wood, J.R., Wilmshurst, J.M., 2012. Wetland soil moisture complicates the use ofSporormiella to trace past herbivore populations. Journal of Quaternary Science27, 254–259.

Yeloff, D., Charman, D., van Geel, B., Mauquoy, D., 2007. Reconstruction of hydrology,vegetation and past climate change in bogs using fungal microfossils. Review ofPalaeobotany and Palynology 146, 102–145.

Yurchenko, E.O., 2001. On some wood-inhabiting dematiaceous hyphomycetes withremarkable conidia in Belarus. Mycena 1, 32–54.

Zhao, Y., Sayer, C.D., Birks, H.H., Hughes, M., Peglar, S.M., 2006. Spatial representation ofaquatic vegetation by macrofossils and pollen in a small and shallow lake. Journalof Paleolimnology 35, 335–350.