Modern non-pollen palynomorphs sedimentation along an elevational gradient in the south-central Pyrenees (southwestern Europe) as a tool for Holocene paleoecological reconstruction

Abstract

Non-pollen palynomorphs (NPPs) are microfossils other than pollen and spores from plants found within samples prepared for pollen analyses. Their utility as paleoecological indicators is rapidly growing because of their potential to complement palynological reconstructions of past communities and environments. The study of modern NPP sedimentation patterns using surface samples from different substrates, vegetation types, and environmental conditions is needed to characterize the main environmental and anthropogenic factors involved in establishing ecological gradients. Here, we analyze modern NPP distribution along an elevational transect from the south-central Pyrenees. We use these data to test the potential influence of elevation, vegetation type, sampling sites, and human disturbance on modern NPP distribution and to obtain a NPP modern-analog model, which will enhance further paleoecological interpretations. Our study used the same surface samples obtained in a previous modern-analog palynological study, along an elevational transect from 870 to 2600 m a.s.l. We identified 55 NPPs, including 13 unidentified morphotypes that were described and depicted. Individual NPP analysis and multivariate statistical methods showed that altitude plays a significant role in the NPP distribution along the transect, but other factors such as soil moisture, landscape openness, and grazing intensity also influenced the composition of NPP assemblages. Our results also recognized some characteristic NPP assemblages linked to elevational vegetation belts and individual NPP morphotypes related with specific microhabitats, both with potential paleoecological indicator capacity. This work is a first step to improve the knowledge of the NPP’s indicator value in the study area.

Keywords

elevation grazing intensity non-pollen palynomorphs paleoecological indicators Pyrenees sample types

Introduction

Paleoecology is an effective tool to improve predictions on the possible consequences of the current climate change on the biosphere by revealing how organisms and communities respond to past environmental changes (Vegas-Vilarrúbia et al., 2011). Modern-analog studies based on present-day sedimentation patterns along ecological gradients are widely used to calibrate paleoecological proxies in terms of the main environmental factors that drive these responses (Jackson and Williams, 2004). The obtained qualitative and quantitative relationships between modern fossil assemblages and environmental drivers are used to interpret past sedimentary records (Birks and Birks, 1980, 2006). Elevational gradients are specially suited for modern-analog studies as they display significant environmental variations in a relatively small study area (Rull, 2006).

Non-pollen palynomorphs (NPPs) are microfossils other than pollen and spores from vascular plants (mainly fungal spores and mycelia, algal remains, and zoological remains) observed in samples prepared for pollen analyses. The utility of NPP as paleoecological indicators is rapidly growing because of their potential to improve the reconstruction of past communities and environments (Van der Linden et al., 2012; Van Geel and Aptroot, 2006; Van Geel et al., 1994). The use of NPP in paleoecological studies has been scarce as compared with other proxies such as pollen, likely due to the limited knowledge about NPP ecological indicator value. However, during the last years, the use of NPP in Quaternary paleoecology has increased and is now a promising and expanding research. It has been shown that NPP studies can enhance paleoecological interpretations based on pollen and pteridophytes spores because of their independent ecological nature (Montoya et al., 2012). This means that NPP and pollen can be conditioned by different variables, as well as they can respond in a different manner to the same factors. In this sense, NPP studies can provide complementary and straightforward information about local effective moisture (Van Geel, 2001) or the effect of livestock on landscape (Cugny et al., 2010; Ejarque et al., 2011) and, in general, significant features of the particular habitat from where samples are collected (Montoya et al., 2010). The use of NPP in paleoecology has been mainly developed in Europe (Buurman et al., 1995; Van Geel, 1978; Van Geel and Aptroot, 2006; Van Geel et al., 2003) and also in South America (e.g. Medeanic, 2006; Montoya et al., 2010, 2011, 2012; Musotto et al., 2012; Rull and Vegas-Vilarrúbia, 1997, 1999, 2001; Rull et al., 2008), Africa (e.g. Ekblom and Gillson, 2010; Gelorini et al., 2011; Van Geel et al., 2011), Asia (De Klerk et al., 2009), and Australia (Cook-Ellyn et al., 2011).

In the Iberian Peninsula, NPP studies are scarce but widespread (Figure 1a). In the Pyrenees, NPP surveys have been mostly oriented to reconstruct historical anthropogenic influences on landscape shaping using sedimentary sequences from fens (Ejarque et al., 2009, 2010; Miras et al., 2010), lakes (Ejarque, 2013; Riera et al., 2006), and peat bogs (Cugny et al., 2010). In general, heterogeneous patterns of landscape evolution during prehistoric and proto-historical times have been documented for highlands. Interactions among environmental, cultural, demographic, and economic drivers seem to be crucial to understand landscape and land-use dynamics in this region (Miras et al., 2010). Of the NPP surveys carried out in the Pyrenees, only two deal with modern analogs. Ejarque et al. (2011) analyzed highland’s modern assemblages of pollen and NPP and found useful relationships with vegetation and environmental patterns, as well as with grazing activities. The study included samples from cattle excrements in order to identify potential grazing indicators. Cugny et al. (2010) analyzed NPP assemblages from moss samples and obtained relevant insights on the degree of the landscape openness, current land-uses, and grazing pressure. This information was successfully applied to a fossil sequence from a peat bog situated in the same area.

Figure 1.

(a) Location of studies that included NPP in the Iberian Peninsula. The present study is marked by a box. White circles are Holocene reconstructions, and black circles are modern-analog studies. Articles, including both types of studies, are indicated by a white circle outside the black one. (1) Asturias (López-Merino et al., 2010, 2011); (2) Gredo’s range, Central Mountain System (Currás et al., 2012; López-Merino et al., 2009); (3) northern-central littoral Portugal (Danielsen, 2008); (4) Cádiz (López-Sáez et al., 2002); (5) southeast of Iberian Peninsula (Carrión and Navarro, 2002); (6) eastern Pyrenees (Ejarque, 2013; Ejarque et al., 2010, 2011; Miras et al., 2010); (7) eastern pre-Pyrenees (Ejarque et al., 2009, 2011); (8) western pre-Pyrenees (Riera et al., 2006); (9) western Pyrenees (Cugny et al., 2010); (10) northeastern Iberian coasts (López-Sáez et al., 2009); and (11) western Catalonia and northern Guadalajara (Currás, 2012). Map source: XTEC (Enrique Alonso). (b) Schematic map of the sampling sites location (black dots). Open dots correspond to towns and the highest mountains are represented by triangles. Gray dots indicate the location of two Holocene cores, currently under study (redrawn from Cañellas-Boltà et al. (2009)).

In this paper, we analyzed the NPP spectra from surface samples along an elevational transect from Vall d’Aran, in the south-central Pyrenees (Figure 1), to test the effects of elevation and other environmental variables. We used the same set of samples used in the study by Cañellas-Boltà et al. (2009), which studied modern analogs of pollen and pteridophyte spores and obtained significant relationships with elevation and vegetation types. Both NPP and pollen/spores were compared to highlight the additional contributions of NPP useful for paleoecological reconstruction. The specific objectives were to (1) characterize the NPP present and their distribution along the elevational transect (from 868 to 2585 m), (2) determine the main factors involved in the NPP distribution (elevation, vegetation type, local habitat, sample type), (3) characterize indicators for specific environmental conditions, and (4) obtain information that will improve the interpretation of NPP extracted from the sediment records in the Pyrenees. Recent modern-analog studies on other mountain ranges have shown that, in general, local elevational transects from around the paleoecological targets, rather than widespread surveys, are better for reliable past reconstructions (Rull, 2006).

Study area

A detailed description of the study area can be found in Cañellas-Boltà et al. (2009). In this paper, the most important aspects of mainly climate and vegetation will be emphasized. Samples analyzed in this work were from the south-central Pyrenees (Vall d’Aran, northwest Catalonia), in the northern peripheral zone of the National Park ‘Aigüestortes i Estany de Sant Maurici’ (Figure 1). Climate is of the Atlantic type with moderate to high precipitation and no water deficit throughout the year (López and Majoral, 1982). Average annual precipitation ranges from 900 to 1200 mm with two maxima, one in the spring (April–March) and the other in autumn (November). Average annual temperatures are generally cool, between 9.5°C (Viella, 974 m) and 2.7°C (Port de la Bonaigua, 2200 m), varying at a rate of −0.55°C/100 m elevation (De Bolòs, 1994). Biogeographically, the studied area is mainly within the boreoalpine and eurosiberian zones, with some Mediterranean elements at the lower parts. The vegetation of Vall d’Aran shows three main altitudinal belts, namely, montane, subalpine, and alpine. In the studied transect (Figure 2), Cañellas-Boltà et al. (2009) described the vegetation gradient as follows:

Montane belt (below 1600 m). Characterized mainly by deciduous oak forests dominated by Quercus petraea with birch (Betula pendula); riverine forests (Alnus glutinosa, Fraxinus excelsior, and Salix sp.); forests with Tilia platyphyllos, Prunus avium, and Corylus avellana; and mixed forests dominated by beech (Fagus sylvatica) with pine (Pinus sylvestris). This lower belt is characterized by the presence of anthropic pressure evidenced by towns, pastures, and cultivation.

Subalpine belt (between 1600 and 2250 m). Dominated by coniferous forests of two types: Abies alba and Rhododendron ferrugineum at the lowest parts and Pinus mugo ssp. uncinata with R. ferrugineum at the upper stages. Wetlands within this belt are characterized by Scirpus cespitosus communities; assemblages of Juncus pyrenaeus, Carex rostrata, and Caltha palustris with Epilobium palustre; and Sphagnum peat bogs. In the region under study, the transition zone between coniferous forests and alpine meadows is at 2000–2250 m and is characterized by scrubs of Rhododendron sp. with scattered pines (P. mugo ssp. uncinata) and patches of Nardus sp. In our transect, the uppermost forest limit (treeline) is situated at 2250 m.

Alpine belt (above 2250 m). Open and sparse vegetation dominated by meadows of Nardus stricta and Festuca eskia, with several species of Carex in the wettest areas.

Figure 2.

Sketch of the altitudinal arrangement of vegetation and the three main belts defined in the studied transect. Numbers at the right side are the sampling codes.

Until mid-1900s, the human activities in the region were cattle raising – mainly cows, sheep, goats, and, to a lesser extent, horses – and forest exploitation and management. Hydroelectricity generation was also a common activity and dam building proliferated. The second half of the past century was characterized by a spectacular increase in tourism activities and an intense emigration of local population to large cities. At present, transhumance seems to experience a revival, and livestock from other Pyrenean areas use to pasture in the Vall d’Aran meadows. However, focus has clearly shifted toward tourism, which has resulted in an increase in urbanization (roads, buildings, etc.), mainly in the montane zone but also in the subalpine and alpine belts by a significant growth of ski stations, with the corresponding increase in deforestation practices. It is noteworthy that an important part of the sampling area belongs to the northern peripheral zone of the National Park ‘Aigüestortes i Estany de Sant Maurici’. This area is under protection, but some human activities, as for example mushroom gatherings, hunting, fishing, hiking, skiing, pasturing, and forest exploitation, are allowed under the corresponding administration control.

Materials and methods

This work used 33 moss samples collected and processed by Cañellas-Boltà et al. (2009). These samples were distributed along an altitudinal transect ranging from 868 (A-32) to 2585 m (A-22; Figures 1 and 2). Moss polsters were chosen as sampling material because they are the only palynomorph traps regularly present along the whole altitudinal transect (lakes and peat bogs are located mainly on the alpine zone). In addition, mosses effectively capture the pollen grain and other microfossils like the NPP and include both local and extra-local representatives, thus becoming suitable palynomorph traps for this type of studies (Birks and Birks, 1980; Wilmshurst and McGlone, 2005). Mosses have been often and successfully used in modern-analog studies on pollen (Court-Picon et al., 2006; Mazier et al., 2006) and on NPP (Ejarque et al., 2011; Montoya et al., 2010). In each sampling site, 2–4 moss fragments of different species were collected and mixed to obtain one single sample. The local and regional flora and vegetation of each location were carefully described using Braun–Blanquet phytosociological methods (Cañellas-Boltà et al., 2009). Tablets of Lycopodium spores were added to each sample, to control the efficiency of chemical processing and to estimate palynomorph concentrations (Stockmarr, 1971).

Samples were processed according to standard palynological procedures (Chambers et al., 2011; Faegri and Iversen, 1989), including KOH digestion, sieving, HCl and HF digestions, and acetylation. HF digestion was used to follow the same methodology as in fossil samples. After sequential dehydration with ethanol and tert-butanol, samples were mounted and stored in silicone oil. NPP identification was carried out using the available keys (Ellis, 1971, 1976) and atlases (Cugny et al., 2010; Gelorini et al., 2011; Hooghiemstra and Van Geel, 1998; Montoya et al., 2010, 2011; Payne et al., 2012; Van Geel, 2001; Van Geel and Aptroot, 2006; Van Geel et al., 2011). Unknown morphotypes were named using the code IBB (for Institut Botànic de Barcelona) and a sequential number and included in our institutional database with their corresponding descriptions and illustrations. Ecological preferences of the NPP encountered in this study are in Appendix 2. Unidentifiable fungal spores were grouped into a general category and were not considered for statistical analyses. Sample A-12 was also rejected for statistics as it did not contain any identified morphotype. Counting was performed according to the diversity saturation criterion (Rull, 1987). NPP abundances were expressed as a percentage based on the pollen sum, which included all pollen taxa except that from aquatic and semiaquatic plants (Cañellas-Boltà et al., 2009). psimpoll 4.27 was used for diagram plotting. Clustering (Euclidean distance and minimum variance agglomerative method) and correspondence analysis (CA) were carried out with MVSP 3.1 (Kovach, 1989) after root square transformation of percentages. Rare taxa were not downweighted.

Results

A total of 55 NPP morphotypes were encountered, corresponding to fungal remains, zoological remains, and algal remains (Table 1). Two of these morphotypes, IBB-255, described here, and IBB-42 previously described by Montoya et al. (2011), have an unknown origin. In all, 42 of the recorded NPP morphotypes were identified to some level (Appendix 2), while other 12 fungal taxa and 1, possibly plant origin (IBB-255), have not been identified so far. These 13 morphotypes were codified using the IBB system, depicted, and described (Appendix 2). The altitudinal distribution of fungal, zoological, and algal groups as a whole is shown in Figure 3. In general, the most abundant NPP were fungal spores, showing little altitudinal differentiation in terms of total abundance. However, the diversity showed more variability, with the highest values in the montane belt (Table 1). Zoological remains were very scarce and almost restricted to the lower parts of montane and subalpine belts, whereas algae only appeared at the lower part of the alpine zone. Below, we analyze the altitudinal distribution of these groups in detail.

Table 1.

Number of morphotypes, percentage of the total NPP, and NPP diversity expressed in a number of identified morphotypes per vegetation zone, based on their origin. ‘Other’ includes IBB-255 and IBB-42, with an unknown origin.

	Zoological remains	Algal remains	Others	Fungal remains
No. of morphotypes	7	1	2	45
% of total NPP	12.73	1.82	3.63	81.82
Alpine	2	1	0	18
Subalpine	5	0	2	27
Montane	2	0	0	31

Figure 3.

Percentage diagram of NPP’s main groups. Vegetation zones, sample code, and sample elevations are shown at the left side. Within the subalpine belt, we highlighted the transition zone (TZ).

Zoological remains, algal remains, and others

Seven zoological morphotypes were recognized corresponding to thecamoebas (3), rotifers (1), turbellarians (1), chironomids (1), and cladocerans (1). Generally, zoological morphotypes were concentrated below 1978 m and were virtually absent above this altitude (Figure 4). Higher abundances as a group occurred at the bottom of the subalpine belt, where it reached its maximal values (sample A-26, 1711 m), as well as in the upper montane zone. The main element was the tecamoeba Assulina sp., occurring at two discontinuous zones: the basal montane belt (868–994 m), and the transition between montane and subalpine belts (1362–1910 m), being responsible for the maximum values of sample A-26 (1711 m). Above this elevation, Assulina sp. occurred only at the base of the alpine belt (2276 m) and disappeared above this point. Most components of this group (Neorhabdocoela sp., Cladocera, Callidina sp., and Amphitrema flavum) showed a similar pattern, being only present between 1825 and 1978 m, within the lower subalpine belt. Chironomid remains appeared only in the uppermost sample (2585 m), while the tecamoeba Centropyxis aculeata was present only in the lowermost sample (868 m), both with very low values.

Figure 4.

Percentage diagram of zoological and algal remains and others, following the same graphical display as in Figure 3.

Pediastrum (Chlorophyta) was the only algal morphotype present in the studied transect, appearing with very low abundances in two samples of the lower alpine zone, below 2280 m (Figure 4). The unknown IBB-255, likely of plant origin, appeared exclusively in the subalpine belt, between 1644 and 2075 m with low to moderate values, with a maximum at 1980 m (Figure 4).

Fungal remains

A total of 45 fungal morphotypes were recorded, showing a much greater diversity and more continuous distribution than the other two groups (Table 1 and Figure 3). Higher values, as a group, occurred in the montane belt, with an absolute maximum at c. 1300 m, as well as in the alpine belt. Lowermost values occurred at the transition between montane and subalpine belts and also in the whole subalpine zone. The montane belt holds the highest fungal diversity with 31 taxa (Table 1). The most abundant morphotype was the unknown IBB-261 (likely belonging to the order Xylariales), although it appeared in a single sample of the mid-montane belt (Figure 5). Also in the montane zone, morphotypes showing significant values were Sordaria-type, IBB-3, Glomus sp., and Clasterosporium sp., whereas Brachysporium bloxamii, Sporormiella sp., cf. Trichocladium sp., Cercophora-type, and cf. Paratomenticola lanceolatus showed lower values (Figure 5). In the subalpine zone, Sordaria-type, IBB-3, and Glomus sp. showed a decrease in their values and Clasterosporium sp. disappeared. Contrarily, Sporormiella sp., Cercophora-type, Podospora sp., and Apiosordaria verruculosa were among the more abundant, together with the unknown IBB-264 and IBB-266, which only occurred in single samples of this zone. The alpine belt showed the lowest fungal diversity of the whole transect (Table 1), but it contained a characteristic group of fungal remains that did not occur at lower elevations (IBB-265, HdV-495, Byssothecium spp., and Arthrinium luzulae). The upper alpine belt was dominated again by Sporormiella sp. and Sordaria-type while UG-1106 increased their values and Glomus sp. disappeared.

Figure 5.

Percentage diagram of fungal remains, following the same graphical display as in Figure 3. Fungal morphotypes have been ordered sequentially according to elevation.

Statistical analysis

Cluster analysis classified the NPP morphotypes into three main groups and four subgroups (Figure 6a), whose altitudinal distribution is also shown (Figure 6b). Group 1 was formed by two coprophilous morphotypes such as Sporormiella sp. and Sordaria-type and was distributed quite continuously throughout the transect, although their maximum values occurred in montane and alpine belts. Group 2 included four fungal types with diverse ecological requirements such as coprophilous-like (Cercophora-type) and mycorrhizic (Glomus sp.). Two additional unknown morphotypes (IBB-261 and IBB-3) were also within this group, which was present in all three vegetation belts but in a more discontinuous manner. Maximum abundances of group 2 were in the mid-montane belt. Group 3 was the most diverse assemblage and contained 49 taxa distributed into four subgroups. Subgroup 3A included two morphotypes (cf. UG-1106 and Byssothecium spp.), distributed almost exclusively in the alpine zone and the uppermost subalpine belt. Subgroup 3B was entirely formed by fungal spores and was especially important in the montane zone where its maximum abundances were recorded. Subgroup 3C was highly heterogeneous including a wide range of morphotypes of different origin. Indeed, it contained all zoological morphotypes except Assulina sp., the alga Pediastrum sp., and a large array of fungal spore types. This subgroup was more or less homogeneously distributed along the transect. Subgroup 3D was formed exclusively by Assulina sp., whose altitudinal distribution has been already described (section ‘Zoological remains, algal remains, and others’).

Figure 6.

NPP assemblages: (a) results of cluster analysis and (b) percentage diagram of the groups obtained in the cluster analysis, following the same graphical display as in Figure 3, and ordered sequentially according to elevation.

Figure 7a shows the results of CA, displaying the analyzed samples in a biplot of the first two axes accounting for 24.9% of the total variance. The first axis (14.7% of the total variance) roughly separated samples collected in forests of several types, situated on the positive side, from samples taken in peat bogs, marshes, wetlands, and meadows, on the negative side. However, five forest samples were situated in the negative side thus disrupting the pattern. These samples were from (1) abandoned crops secondarily colonized by deciduous woody vegetation very rich in Brachypodium sylvaticum (Poaceae; A-29), (2) open conifer forests of P. mugo ssp. uncinata with R. ferrugineum (A-9), (3) light hazel (C. avellana) forests with marginal vegetation and close to a town (A-3), (4) riverine forests on flooded soils surrounded by open vegetation (A-2), and (5) ash (F. excelsior) forests rich in B. sylvaticum in the surroundings of a small town (A-1; see Appendix 1). In general, samples from alpine and subalpine belts were placed at the negative side of axis 1, while samples from montane belt were mostly at the positive part. All samples belonging to the transition zone (A-13, A-14, A-15, and A-25) lie within the subalpine samples, situated at the negative side of axis 1. The Pearson product–moment correlation coefficient between sample elevation and the scores of axis 1 is r = −0.442, which is significant at p < 0.02. Axis 2 explained 10.2% of the total variance and did not show a clear pattern in the distribution of the samples. However, spring vegetation, wetlands, and some peat bogs and marshes were consistently situated at the positive half, whereas samples taken at more rocky and less humid environments (Appendix 1) were situated at the negative side.

Figure 7.

Correspondence analysis (CA). (a) Results of CA showing the arrangement of the 32 sample sites, in the space defined by the two first axes. Locations have been differentiated according to the habitat and the altitude (see legend). ‘Other’ includes different vegetation types: meadows (A-13 and A-23), wetlands (A-8), streams between rocks (A-11), and snow banks (A-21). Samples with the highest values of Sporormiella sp. and Sordaria-type (cluster group 1) are marked with an asterisk. Samples from the forest/meadows transition zone are underlined. (b) Results of CA showing the arrangement of the 55 NPP morphotypes types using the first two axes. NPP have been differentiated according to their origin and their ecologic preferences (Appendix 2). ‘Other fungi’ include morphotypes with no defined autoecological preferences and ‘Others’ include NPP of unknown origin (IBB-255 and IBB-42). Numbers correspond to Coniochaeta cf. ligniaria (1) and Assulina sp. (2).

Figure 7b shows the distribution of the NPP morphotypes along the first two CA axes. Axis 1 separated Assulina sp., situated at the positive side, from the other zoological remains, which are around the center of the plot. Assulina sp. coincides with most samples from densely forested sites (Figure 7a). Fungi are arranged along axis 1 as well, with coprophilous forms grouped at the negative side and most saprobic morphotypes placed at the positive part. NPP arrangement along axis 2 does not show any conspicuous pattern.

Discussion

NPP and elevation

In mountain areas, elevation is intimately linked to keystone climatic parameters as, for example, annual average temperatures and total precipitation. Therefore, paleoaltitude estimations from palynomorph assemblages based on modern-analog comparisons may provide relevant paleoclimatic information (Rull, 2006). In our transect, previous studies showed a highly significant correlation (r = 0.988, p < 0.001) between pollen trends and elevation (Cañellas-Boltà et al., 2009). According to the results of this study, NPP-elevation correlation using the same methodology are remarkably lower, although statistically significant (r = −0.442, p < 0.02). Therefore, elevation may explain in part the altitudinal NPP distribution, but other independent factors should be invoked to fully account for the observed trends. As previously shown, the arrangement of samples along CA axis 1 follows an altitudinal-like trend with some exceptions, notably the presence of samples from montane and subalpine zones within the alpine group (Figure 7a), indicating that this axis may represent not only elevation but also other factors. For example, samples located at the negative side are mostly from meadows and marshes – excepting five samples from relatively open forests – while samples at the positive side were taken in forested areas, suggesting a gradient of landscape openness from right to left. In concordance to this, coprophilous fungi, which are dominant in open grazed sites, are mostly placed at the negative side of the CA axis 1, whereas saprobic fungi and Assulina sp., mostly from forested sites, are situated at the positive part (Figure 7b). In addition, all samples with high values of Sporormiella sp. and Sordaria-type (group 1; samples A-3, A-13, A-18, A-22, A-24, and A-29, Figure 7a), including some forested sites (A-29 and A-3), are in the negative side of this axis. On the other hand, all samples placed at the positive side, especially those with the highest positive scores of axis 1 (A-4, A-26, A-27, and A-28), show low values for coprophilous fungi. Therefore, axis 1 also could suggest a grazing gradient linked to landscape openness (see section ‘NPP and human pressure’). Axis 2 provided additional information such as samples from moist or flooded habitats were at the positive side, whereas samples at the negative values come from less humid rocky soils (Appendix 1), thus suggesting a likely moisture gradient. Therefore, in addition to elevation, landscape openness and soil moisture gradients are also relevant to account for the features of the NPP spectra analyzed. Other works developed on the Pyrenees also showed a variety of factors influencing NPP assemblages. For example, Court-Picon et al. (2006) found that elevation was the more important environmental driver, whereas Cugny et al. (2010) emphasize the role of grazing pressure, regardless of the altitude and the local habitat conditions. Ejarque et al. (2011) suggested that elevation did not play a significant role in the composition of NPP assemblages, the features of which were more related to sample type, landscape openness, and grazing pressure. Taken individually, some of the NPP groups obtained in the cluster analysis show elevational trends while others do not. For example, subgroups 3B and 3D are indicators of lower elevations, while subgroup 3A is typical of the uppermost levels of the transect (Figure 6b). Therefore, these subgroups could be useful for paleoecological and paleoclimatic reconstructions.

NPP and vegetation

Some associations between specific groups of NPP and vegetation belts are evident. For example, IBB-256, IBB-261, Clasterosporium sp., and cf. B. bloxamii characterize the montane zone, whereas IBB-264, HdV-65, IBB-255, and IBB-263 only occur in the subalpine zone. Byssothecium spp. is exclusive of the alpine zone only. These relationships could be used as indicators in further paleoecological studies. Another important issue, from a paleoecological point of view, is the position of the upper limit of the forest (treeline). Variations in the elevation of the treeline may be climatically controlled and can provide insights into paleotemperatures and paleoprecipitation. In our transect, the transition zone between pine forests and alpine meadows (2000–2250 m) was previously characterized palynologically by a significant increase in Cyperaceae and Poaceae (Cañellas-Boltà et al., 2009). In the case of NPP, this zone is less well defined, although some peculiarities have been observed. This transition zone is characterized by the disappearance of IBB-255 and almost all the zoological remains, especially Assulina sp., and by an increase of fungal spores, specifically Sporormiella sp. and Sordaria-type (Figures 3 –5). Immediately above the uppermost forest boundary (2250 m), Byssothecium spp. appears and increases their abundances progressively with elevation. In summary, NPP can contribute to locate the position of the treeline and its variations through time in the studied zone, which is encouraging for paleoecological reconstructions. It should be noted, however, that the treeline location may be influenced not only by climatic changes but also by human activities, which complicates past inferences. However, it is expected that human activities associated with treeline variations would be manifested in other indicators (charcoal from fires, pollen from cultivated plants, NPP as indicators of grazing, etc.), thus allowing separation of natural from anthropic drivers.

Some relationships exist among individual NPP and some forest communities that would be relevant for paleoecological interpretation. For example, Assulina sp., a tecamoeba typical of non-saturated moss polsters (Charman et al., 2000), occurs at two elevational bands, namely, the lowermost montane belt and the montane/subalpine transition (Figure 4), always in forest samples (Appendix 1). In the montane zone, Assulina sp. occurs in deciduous and mixed forests (A-31, A-32, and A-33), whereas in the montane/subalpine transition (from 1362 to 1749 m), this tecamoeba is only present in mixed (A-4, A-27, and A-28) and coniferous forest samples (A-5, A-6, and A-26). It is also noteworthy that in the montane belt, Assulina sp. is absent from moist riverine forests surrounded by open vegetation (A-1 and A-2), from small stream between old hayfields and forested patches (A-11) and also from three highly anthropic and relatively open sites (A-3, A-29, and A-30). These three samples also have high values of dung-related fungi (Sporormiella sp., Sordaria-type, and Cercophora-type). Therefore, this tecamoeba would be associated with the presence of deciduous, mixed, and coniferous forests growing on non-flooded soils, avoiding low forested and/or heavily grazed sites. Similar results were obtained by Ejarque et al. (2011), who related this morphotype to poorly grazed pine forests with abundant mosses in the understory. Another coincidence to be considered involves the unknown IBB-255, only present in coniferous forests of P. mugo ssp. uncinata and A. alba. Cluster analysis grouped IBB-255 with Trichocladium sp., cf. B. bloxamii and cf. P. lanceolatus, which used to grow on wood and bark from a variety of forest trees (Ellis, 1971; Shirouzu and Harada, 2008). Other relationships are less clear, but they are worth mentioning to be confirmed in future studies. For example, IBB-3 and IBB-261 are particularly abundant in samples from C. avellana and F. sylvatica forests of the montane belt, both with a thick litter layer on the soil (Appendix 1). These morphotypes might correspond to plant remain decomposers, but further studies are needed for a definite assessment.

Also relevant is the occurrence of IBB-266 in one single sample from the alpine belt. This morphotype likely belongs to Cortinarius (Agaricales), some of which species have mycorrhizal relationships with the dwarf willow Salix herbacea in the alpine zone (Mühlmann and Peintner, 2008). S. herbacea is a boreoalpine species common in the uppermost levels of the Pyrenean alpine belt, where it grows around snow smelt banks (Vigo, 2005), and was found by Cañellas-Boltà et al. (2009) at the same altitudinal level as the sample in which IBB-266 occurs. Therefore, IBB-266 would be indicator not only of the uppermost alpine belt but also of the presence of S. herbacea.

NPP and sample type

In general, the diversity and abundance of zoological and algal remains recorded in this survey are comparatively low. Pediastrum sp. is the only algal representative found and is only present in two alpine samples along the whole transect. The presence of springs and water bodies around these sampling sites could explain the appearance of Pediastrum sp. at this altitude (Appendix 1). Pediastrum is a genus of colonial green algae that lives in different freshwater habitats (Komárek and Jankovská, 2001). Depending on the species, Pediastrum can be common in the plankton from eutrophic lakes, as well as in the littoral zone from oligotrophic water bodies (Weckström et al., 2009). As a NPP, maximum Pediastrum abundances occur in peat bogs and lake sediments (Montoya et al., 2010). Therefore, the scarcity of this morphotype in the Pyrenean transect studied here could be due to the use of mosses as sampling material. The same would be true for zoological remains, as most of the usually found in pollen slides are from aquatic or semiaquatic habitats (Charman et al., 2000; Haas, 1996; Korhola and Rautio, 2001; Walker, 2001). Further studies should analyze a wider range of sample types, in order to complement our results on modern NPP sedimentation. The combined study of samples from mosses, wet soils, and lake and bog sediments is needed to properly evaluate the local factors influencing NPP assemblages (Montoya et al., 2010), in order to obtain more useful paleoecological indicators. However, as stated in the ‘Materials and methods’ section, the handicap is that bogs and lakes are usually restricted to higher elevations, and their altitudinal distribution is not as continuous as moss polsters.

NPP and human pressure

Sporormiella sp. and Sordaria-type are typical of cattle dung (Ejarque et al., 2011; Gauthier et al., 2010; Van Geel and Aptroot, 2006) and are commonly used as indicators of grazing pressure in the Pyrenees (Cugny et al., 2010; Ejarque et al., 2011) and elsewhere. In our transect, although these taxa appear along the whole elevational gradient, their maximum values occur in alpine meadows dominated by herbaceous vegetation and close to water bodies (Appendix 1), which are sites prone to be visited by cattle. In addition, Sordaria-type shows high values in the montane belt in three forested sites, either covered by a hazel forest (A-3) or close to abandoned crops colonized by T. platyphyllos, P. avium, and C. avellana (A-29 and A-30). These sites include relatively open forests rich in fruits, and herbivory is also favored. In addition to Sordaria-type, these samples hold relatively high values of other two coprophilous fungi (Sporormiella sp. and Cercophora-type), strongly suggesting the presence of herbivore grazing in these three sites. Cañellas-Boltà et al. (2009) did not find palynological evidence of cultivation or grazing activities and concluded that there was no clear evidence of human disturbance. However, the relatively high abundances of coprophilous NPP (Sordaria-type and Sporormiella sp.) in several parts of the studied transect suggest local grazing. On the other hand, Sordaria-type and Sporormiella sp. form a distinct group on cluster analysis (Figure 6a) showing their maximum abundances at open and grazed sites. This coincides with the observations by Ejarque et al. (2011) and Cugny et al. (2010), who suggested that the mentioned fungi are good grazing indicators. On the contrary, Coniochaeta cf. ligniaria, growing on decomposed wood and dung (Appendix 2), is placed at the positive side of CA axis 1 (Figure 7b) together with most saprobic fungi, suggesting that this morphotype may be a suitable indicator for litter accumulation. On the other hand, Glomus sp. spores have their maximal values in several forested sites from the montane belt, in contrast with the greater abundance of this taxon in subalpine meadows from other Pyrenean areas (Ejarque et al., 2011). In our transect, the highest values of Glomus occur in samples from forested sites close to pathways and forest tracks built mainly for touristic and recreation purposes. This agrees with studies from elsewhere showing that high abundances of this endomycorrhizal fungus in surface samples have been related to increased erosive phenomena and other mechanical soil disturbances (Van Geel et al., 1989). Therefore, the occurrence and abundance of spores from coprophilous fungi and Glomus sp. suggest that the studied region, despite the official protection as the peripheral zone of a national Park, is under certain degree of human pressure, mainly related to grazing and tourism, which are manifest throughout the whole transect. As a consequence, human pressure should be added to elevation, vegetation type, landscape openness, and local moisture conditions, as one more environmental driver controlling the NPP distribution along the studied transect.

Conclusion

The study of NPP assemblages along an elevational transect from south-central Pyrenees using moss samples revealed that fungal spores were, by far, more diverse and abundant than algal and zoological remains. A total of 55 morphotypes were found, of which 13 were described and depicted for the first time. Our results suggest that elevation have a significant influence on the NPP distribution in the studied region, but other factors such as soil moisture, vegetation type, landscape openness, and grazing pressure are also influencing. These factors, however, are not totally independent from elevation, thus determining a complex altitudinal pattern. Useful relationships between NPP assemblages and specific vegetation belts have been recognized. Also, the transition zone between subalpine to alpine belts (treeline) has been characterized on the basis of NPP assemblages. The low diversity and abundance of zoological and algal remains were likely due to the lack of lake and bog samples in the transect. This NPP study has been able to find signs of anthropogenic disturbance (notably soil erosion and grazing), previously unnoticed by palynological analyses, emphasizing the utility of NPP to obtain more thorough paleoecological reconstructions. This work should be considered the starting point to improve the knowledge of the NPP indicator capacity in the study area, aimed to improve further paleoecological interpretations. Further studies should increase the number of transects, considering several differential conditions (geology, slope exposure, degree, and type of human disturbance), and enhance sampling types, including surface sediments from peat bogs, marshes, and lakes. Next step should be to test the paleoecological utility of the modern analogs obtained in this study, in sedimentary sequences obtained in the same transect.

Footnotes

Appendix 1

Sample	Altitude (m)	Vegetation features	Main plant composition	Coordinates UTM
A-22	2585	Herb bog near a pond, surrounded by granite boulders	Carex pyrenaica, Nardus stricta, Saxifraga stellaris, Veronica alpina	42°35′58″N; 0°55′58″E
A-23	2542	N. stricta meadow	N. stricta, C. pyrenaica, Gentiana alpina, Gnaphalium supinum, Saxifraga stellaris	42°36′1″N; 0°55′52″E
A-21	2536	Herb patch close to a permanent snow bank beneath large rock blocks	Luzula alpinopilosa, Salix herbacea, N. stricta, Sibbaldia procumbens	42°36′58″N; 0°56′9″E
A-24	2488	Acidic herb bog near a small stream	Carex nigra, Juncus filiformis, N. stricta, Saxifraga stellaris	42°36′N; 42°37′44″E
A-20	2458	Acidic herb bog on rocky soil dominated by C. nigra, at the shore of a pond and close to a spring	C. nigra, Carex echinata	42°36′7″N; 0°56′23″E
A-19	2398	Acidic herb bog surrounded by small streams and large rock blocks	C. nigra, Viola palustris, C. echinata, N. stricta, Saxifraga stellaris	42°36′21″N; 0°56′27″E
A-17	2331	Herb bogs at both sides of a small stream	Edges of the small stream: Scirpus cespitosus, Carex gr. flava, Festuca gr. rubra; meadow: Festuca eskia, Festuca gr. rubra, N. stricta	42°37′8″N; 0°54′28″E
A-16	2280	Herb bog close to a small spring and stream, situated at the upper boundary of Pinus mugo ssp. uncinata	Spring and herb bog: C. nigra, C. gr. flava, Scirpus cespitosus, Juncus alpinus	42°37′14″N; 0°54′27″E
A-18	2276	Acidic herb bog close to a small pond, surrounded by pastures on rocky substrate	Herb bog: Scirpus cespitosus; meadow: Calluna vulgaris, Molinia caerulea, N. stricta, Primula integrifolia	42°37″N; 0°55″E
A-15	2240	Small springs among granitic blocks, surrounded by herb bogs and meadows	At the springs: Saxifraga stellaris, C. nigra, Epilobium alsinifolium; herb bog: C. nigra, Scirpus cespitosus; meadow: Festuca gr. rubra, N. stricta, C. nigra, Primula integrifolia	42°37′16″N; 0°54′46″E
A-14	2176	C. nigra bog near a stream and some small ponds	Herb bog: C. nigra, Leontodon duboisii, Parnassia palustris, Viola palustris; wet meadows: N. stricta, Festuca gr. rubra, Trifolium repens, Poa supina, Selinum pyrenaeum; among granitic blocks: Rumex pseudoalpinus, Festuca eskia, Athyrium distentifolium	42°37′20″N; 0°55″E
A-13	2116	Vegetation mosaic at both sides of a stream	C. sempervirens spp. pseudotristis, Alchemilla coriacea, C. nigra, Deschampsia cespitosa, Festuca eskia, Festuca rivularis, L. alpinopilosa, Parnassia palustris	42°37′31″N; 0°55′10″E
A-25	2075	Slightly alkaline herb bog near a small stream of quiet waters	Narthecium ossifragum, Scirpus cespitosus, Carex davalliana	42°37′44″N; 0°55′27″E
A-12	2036	Shore of a small pond	Small pond: Carex rostrata; edges of the small pond: C. nigra, Viola palustris, Potentilla erecta, Succisa pratensis; outside the pond: acidic wet meadow: Festuca rubra, N. stricta, Potentilla erecta, Succisa pratensis, Luzula multiflora, Selinum pyrenaeum	42°37′48″N; 0°55′33.7″E
A-9	1980	Light woods of Pinus mugo ssp. uncinata with Rhododendron ferrugineum on granitic soil	R. ferrugineum, Homogyne alpinus, Pinus mugo ssp. uncinata, Solidago virgaurea, Vaccinum uliginosum	42°38′17″N; 0°55′18″E
A-8	1978	Herb bog at both sides of a small stream, surrounded by rush	C. gr. flava, Juncus pyrenaeus, Carex panicea, Cirsium rivulare, D. cespitosa, Succisa pratensis	42°37′58″ N; 0°55′12″E
A-10	1910	Floating bog on a small pond	Sphagnum sp., Carex lasiocarpa, Drosera longifolia, Menyanthes trifoliata, M. caerulea, Parnassia palustris	42°38′17″N; 0°55′29″E
A-7	1825	Scirpus cespitosus community and herb bogs	Scirpus cespitosus, M. caerulea, Bartsia alpina, D. cespitosa, Equisetum fluviatile, Parnassia palustris, Pinguicula sp.	42°38′46″ N; 0°55′59″E
A-6	1749	Fir forest within large granitic blocks	Abies alba, Populus tremula, Vaccinium myrtillus	42°39′46″N; 0°55′22″E
A-26	1711	Open pine forest	Pinus mugo ssp. uncinata, V. myrtillus, Deschampsia flexuosa, Hieracium cf. Prenanthoides, Melampyrum pratense	42°39′44″N; 0°55′14″E
A-5	1644	Fir forest with R. ferrugineum on granitic soil	A. alba, V. myrtillus, R. ferrugineum, Calamagrostis arundinacea, Oxalis acetosella	42°39′53″N; 0°55′13″E
A-11	1561	Small stream within granitic boulders between old hayfields and forested patches	On both sides of the small stream: Cardamine raphanifolia, Chaerophyllum hirsutum, Caltha palustris, Equisetum arvense, Holcus lanatus; forest partch: Corylus avellana, Betula pendula, Laserpitium latifolium, Lathyrus laevigatus, Pinus sylvestris, Prunella grandiflora; meadow: Centaurea nigra, Agrostis tenuis, Asphodelus albus, Briza media, Carlina cynara, Scabiosa columbaria, Vicia orobus	42°40′28″N; 0°54′48″E
A-27	1495	Birch forest with conifers at the shore of a river	Betula pendula, Pinus sylvestris, Astrantia major, Lathyrus laevigatus	42°40′48″N; 0°54′57″E
A-4	1447	Birch and pine forest colonizing a scree	Betula pendula, Pinus sylvestris, Poa nemoralis, Rubus idaeus, Dryopteris filix-mas	42°41′53″N; 0°54′52″E
A-28	1362	Young mixed forest close to a road	Corylus avellana, A. alba, Fraxinus excelsior, Melica uniflora	42°41′44″N; 0°54′41″E
A-3	1328	Hazel forest on calcareous soil close to a road. Many oak leaves (Quercus petraea) on the ground. There is also open and marginal vegetation	Corylus avellana, Carex ornithopoda, Fraxinus excelsior, Lonicera xylosteum	42°42′7″N; 0°54′27″E
A-2	1226	Riverine willow forest on peaty soil	Salix purpurea, E. arvense, Angelica razulii, Corylus avellana, Fraxinus excelsior, Knautia arvernensis	42°40′59″N; 0°52′29″E
A-29	1152	Abandoned terraces colonized by woody vegetation and some abandoned meadows around them. Close to a town	Brachypodium sylvaticum, Prunus avium, Corylus avellana, Fraxinus excelsior, Geum urbanum	42°41′44″N; 0°52′18″E
A-30	1096	Abandoned crops colonized by Tilia platyphyllos and Prunus avium forest	Corylus avellana, T. platyphyllos, Galium odoratum, Geum urbanum, P. avium	42°41′54″N; 0°50′56″E
A-1	1027	Ash forest in the edge of a river, close to a town and a road	Fraxinus excelsior, Corylus avellana, B. sylvaticum, Crataegus monogyna, Geranium robertianum	42°41′55″N; 0°49′17″E
A-31	994	Acidic pine wood with beech	Fagus sylvatica, Pinus sylvestris, A. alba, Fragaria vesca, Galium rotundifolium	42°43′49″N; 0°46′8″E
A-33	943	Old cultivated terraces colonized by mixed forest, on silicic soil	Q. petraea, Betula pendula, Fraxinus excelsior	42°43′47″N; 0°43′39″E
A-32	868	Mixed forest of alder and ash, with small streams	Alnus glutinosa, Athyrium filix-femina, Carex flacca, Crepis paludosa, Filipendula ulmaria, Fraxinus excelsior, Mercurialis perennis	42°43′56″N; 0°43′14″E

Appendix 2 Acknowledgements

We thank Josep Vigo and Arnau Mercadé for their help in sampling and floristic work, and Jaume Llistosella and the participants of the 5th workshop on non-pollen palynomorphs (University of Amsterdam, 2–4 July 2012) in the identification of several fungal spores. Finally, we are also grateful to the constructive comments and the revision by Will Gosling and by the anonymous referee, who contributed to improve the manuscript.

Funding

This work was included in a project funded by the Institute for Catalan Studies (IEC; principal investigator, V. Rull).

References

Bell

(2005) An Illustrated Guide to the Coprophilous Ascomycetes of Australia (CBS Biodiversity Series, No. 3). Utrecht: CBS.

Birks

HJB

Birks

(1980) Quaternary Paleoecology. Caldwell, NJ: The Blackburn Press.

Birks

HJB

(2006) Multi-proxy studies in palaeolimnology. Vegetation History and Archaeobotany 15: 235–251.

Buurman

van Geel

van Reenen

GBA

(1995) Palaeoecological investigations of a Late Bronze Age watering-place at Bovenkarspel, The Netherlands. Mededelingen: Rijks Geologische Dienst 52: 249–270.

Cañellas-Boltà

Rull

Vigo

. (2009) Modern pollen-vegetation relationships along an altitudinal transect in the central Pyrenees (southwestern Europe). The Holocene 19: 1185–1200.

Carrión

Navarro

(2002) Cryptogam spores and other non-pollen microfossils as sources of palaeoecological information: Case-studies from Spain. Annales Botanici Fennici 39: 1–14.

Chambers

van Geel

van der Linden

(2011) Considerations for the preparation of peat samples for palynology, and for the counting of pollen and non-pollen palynomorphs. Mires and Peat 7: 1–14.

Charman

Hendon

Woodland

(2000) The Identification of Testate Amoebae (Protozoa: Rhizopoda) in Peats (Technical Guide, 9). London: Quaternary Research Association.

Cook-Ellyn

van Geel

van der Kaars

. (2011) A review of the use of non-pollen palynomorphs in palaeoecology with examples from Australia. Palynology 35: 155–178.

10.

Court-Picon

Buttler

de Beaulieu

(2006) Modern pollen/vegetation/land-use relationships in mountain environments: An example from the Champsaur valley (French Alps). Vegetation History and Archaeobotany 15: 151–168.

11.

Cugny

Mazier

Galop

(2010) Modern and fossil non-pollen palynomorphs from the Basque mountains (western Pyrenees, France): The use of coprophilous fungi to reconstruct pastoral activity. Vegetation History and Archaeobotany 19: 391–408.

12.

Currás

(2012) Estudio sobre la evolución de paisajes mediterráneos continentales en Lleida y Guadalajara durante los últimos 3000 años a partir de las secuencias polínicas de Ivars, Somolinos y Cañamares. PhD Thesis, Universitat de Barcelona. Availabe at: http://hdl.handle.net/2445/42650.

13.

Currás

Zamora

Reed

. (2012) Climate change and human impact in central Spain during Roman times: High-resolution multi-proxy analysis of a tufa lake record (Somolinos, 1280 m asl). Catena 89: 31–53.

14.

Danielsen

(2008) Paleoecological development of the Quiaios-Mira dunes, northern-central littoral Portugal. Review of Palaeobotany and Palynology 152: 74–99.

15.

De Bolòs

(1994) Atles comarcal de Catalunya: Val d’Aran. Barcelona: Institut Cartogràfic de Catalunya.

16.

De Klerk

Donner

Joosten

. (2009) Vegetation patterns, recent pollen deposition and distribution of non-pollen palynomorphs in a polygon mire near Chokurdakh (NE Yakutia, NE Siberia). Boreas 38: 39–58.

17.

Ejarque

(2013) La alta montaña pirenaica: génesis y configuración holocena de un paisaje cultural. Estudio paleoambiental en el valle del Madriu-Perafita-Claror (Andorra) (British Archaeological Reports, International Series 2507). Oxford: Archaeopress.

18.

Ejarque

Miras

Riera

(2011) Pollen and non-pollen palynomorph indicators of vegetation and highland grazing activities obtained from modern surface and dung datasets in the eastern Pyrenees. Review of Palaeobotany and Palynology 167: 123–139.

19.

Ejarque

Julià

Riera

. (2009) Tracing the history of highland human management in the eastern Pre-Pyrenees: An interdisciplinary palaeoenvironmental study at the Pradell fen, Spain. The Holocene 19: 1241–1255.

20.

Ejarque

Miras

Riera

. (2010) Testing microregional variability in the Holocene shaping of high mountain cultural landscapes: A palaeoenvironmental case-study in the eastern Pyrenees. Journal of Archaeological Science 37: 1468–1479.

21.

Ekblom

Gillson

(2010) Dung fungi as indicators of past herbivore abundance, Kruger and Limpopo National Park. Palaeogeography, Palaeoclimatology, Palaeoecology 296: 14–27.

22.

Ellis

(1971) Dematiaceous Hyphomycetes. London: The Eastern Press Ltd.

23.

Ellis

(1976) More Dematiaceous Hyphomycetes. Aberystwyth: The Cambrian News Ltd.

24.

Faegri

Iversen

(1989) Textbook of Pollen Analysis. Caldwell, NJ: The Blackburn Press.

25.

Gauthier

Bichet

Massa

. (2010) Pollen and non-pollen palynomorph evidence of medieval farming activities in southwestern Greenland. Vegetation History and Archaeobotany 19: 427–438.

26.

Gelorini

Verbeken

van Geel

. (2011) Modern non-pollen palynomorphs from East African lake sediments. Review of Palaeobotany and Palynology 164: 143–173.

27.

Haas

(1996) Neorhabdocoela oocytes: Palaeoecological indicators found in pollen preparations from Holocene freshwater lake sediments. Review of Palaeobotany and Palynology 91: 371–382.

28.

Hooghiemstra

Van Geel

(1998) World list of Quaternary pollen and spore atlases. Review of Palaeobotany and Palynology 104: 157–182.

29.

Jackson

Williams

(2004) Modern analogs in Quaternary paleoecology: Here today, gone yesterday, gone tomorrow? Annual Reviews of Earth and Planetary Sciences 32: 495–537.

30.

Komárek

Jankovská

(2001) Review of the Green Algal Genus Pediastrum: Implication for Pollen-Analytical Research (Bibliotheca Phycologica, Band 108). Berlin/Stuttgart: J. Cramer.

31.

Korhola

Rautio

(2001) Cladocera and other banchiopod crustaceans. In: Smol

Birks

JHB

Last

(eds) Tracking Environmental Change Using Lake Sediments, Volume 4: Zoological Indicators. Dordrecht; London: Kluwer Academic Publishers, pp. 5–41.

32.

Kovach

(1989) Comparisons of multivariate analytical techniques for the use in pre-Quaternary plant palaeoecology. Review of Palaeobotany and Palynology 60: 255–282.

33.

López

Majoral

(1982) La Vall d’Aran. Medi físic i transformació econòmica. Barcelona: Caixa d’Estalvis de Catalunya.

34.

López-Merino

Martínez

López-Sáez

(2010) Early agriculture and paleoenvironmental history in the North of the Iberian Peninsula: A multi-proxy analysis of the Monte Areo mire (Asturias, Spain). Journal of Archaeological Science 37: 1978–1988.

35.

López-Merino

Martínez

López-Sáez

(2011) Human-induced changes on wetlands: A study case from NW Iberia. Quaternary Science Reviews 30: 2745–2754.

36.

López-Merino

López-Sáez

Alba-Sánchez

. (2009) 2000 years of pastoralism and fire shaping high-altitude vegetation of Sierra de Gredos in central Spain. Review of Palaeobotany and Palynology 158: 42–51.

37.

López-Sáez

López

Martín

(2002) Palaeoecology and Holocene environmental change from a saline lake in south-west Spain: Protohistorical and prehistorical vegetation in Cádiz Bay. Quaternary International 93–94: 197–206.

38.

López-Sáez

López-Merino

Mateo

. (2009) Palaeoecological potential of marine organic deposits of Posidonia oceanica: A case study in the NE Iberian Peninsula. Palaeogeography, Palaeoclimatology, Palaeoecology 271: 215–224.

39.

Marinas

Gómez

García-González

(2009) 6410 Prados-juncales con Molina caerulea sobre suelos húmeros gran parte del año. In: VV.

AA.

(ed.) Bases ecológicas preliminares para la conservación de los tipos de hábitat de interés comunitario en España. Madrid: Ministerio de Medio Ambiente, y Medio Rural y Marino, 54 pp.

40.

Mazier

Galop

Brun

. (2006) Modern pollen assemblages from grazed vegetation in the western Pyrenees, France: A numerical tool for more precise reconstruction of past cultural landscapes. The Holocene 16: 91–103.

41.

Medeanic

(2006) Freshwater algal palynomorph records from Holocene deposits in the coastal plain of Rio Grande do Sul, Brazil. Review of Palaeobotany and Palynology 141: 83–101.

42.

Miras

Ejarque

Orengo

. (2010) Prehistoric impact on landscape and vegetation at high altitudes: An integrated palaeoecological and archaeological approach in the eastern Pyrenees (Perafita valley, Andorra). Plant Biosystems 144: 946–961.

43.

Montoya

Rull

Nogué

(2011) Early human occupation and land use changes near the boundary of the Orinoco and the Amazon Basins (SE Venezuela): Palynological evidence from El Paují record. Palaeogeography, Palaeoclimatology, Palaeoecology 310: 413–426.

44.

Montoya

Rull

van Geel

(2010) Non-pollen palynomorphs from surface sediments along an altitudinal transect of the Venezuelan Andes. Palaeogeography, Palaeoclimatology, Palaeoecology 297: 169–183.

45.

Montoya

Rull

Vegas-Vilarrúbia

(2012) Non-pollen palynomorph studies in the Neotropics: The case of Venezuela. Review of Palaeobotany and Palynology 186: 102–130.

46.

Mühlmann

Peintner

(2008) Mycobionts of Salix herbacea on a glacier forefront in the Austrian Alps. Mycorrhiza 18: 171–180.

47.

Musotto

Bianchinotti

Borromei

(2012) Pollen and fungal remains as environmental indicators in surface sediments of Isla Grande de Tierra del Fuego, southernmost Patagonia. Palynology 36: 162–179.

48.

Payne

Lamentowicz

van der Knaap

. (2012) Testate amoebae in pollen slides. Review of Palaeobotany and Palynology 173: 68–79.

49.

Riera

López-Sáez

Julià

(2006) Lake responses to historical land use changes in northern Spain: The contribution of non-pollen palynomorphs in multiproxy study. Review of Palaeobotany and Palynology 141: 127–137.

50.

Rull

(1987) A note on pollen counting in palaeoecology. Pollen et Spores 29: 471–480.

51.

Rull

(2006) A high mountain pollen-altitude calibration set for paleoclimatic use in the tropical Andes. The Holocene 16: 105–107.

52.

Rull

Vegas-Vilarrúbia

(1997) Acari remains from pleniglacial sediments of the Venezuelan Andes and their paleolimnological significance. Current Research in the Pleistocene 14: 153–155.

53.

Rull

Vegas-Vilarrúbia

(1999) Surface palynology of a small coastal basin from Venezuela and potential palaeoecological applications. Micropaleontology 45: 365–393.

54.

Rull

Vegas-Vilarrúbia

(2001) Paleoecology and paleolimnology of the last Pleniglacial in the Venezuelan Andes. In: Goodman

Clarke

(eds) Proceedings of the IX International Palynological Congress, Houston, Texas, USA, 1996. Dallas, TX: AASP Foundation, pp. 385–401.

55.

Rull

López-Sáez

Vegas-Vilarrúbia

(2008) Contribution of non-pollen palynomorphs to the paleolimnological study of a high-altitude Andean lake (Laguna Verde Alta, Venezuela). Journal of Paleolimnology 40: 399–411.

56.

Shirouzu

Harada

(2008) Lignicolous dematiaceous hyphomycetes in Japan: Five new records for Japanese mycoflora, and proposals of a new name, Helminthosporium magnisporum, and a new combination, Solicorynespora foveolata. Mycoscience 49: 126–131.

57.

Stockmarr

(1971) Tablets with spores used in absolute pollen analysis. Pollen et Spores 13: 615–621.

58.

Van der Linden

Kooistra

Engels

(eds) (2012) Non-pollen palynomorphs as relevant indicators in palaeoecology and archaeobotany. Review of Palaeobotany and Palynology 186: 1–162.

59.

Van Geel

(1976) Fossil spores of Zygnemataceae in ditches of a prehistoric settlement in Hoogkarspel (The Netherlands). Review of Palaeobotany and Palynology 22: 337–374.

60.

Van Geel

(1978) A paleoecological study of Holocene peat bog sections in Germany and The Netherlands, based on the analysis of pollen, spores and macro- and microremains of fungi, algae, cormophytes and animals. Review of Palaeobotany and Palynology 25: 1–120.

61.

Van Geel

(2001) Non-pollen palynomorphs. In: Smol

Birks

HJB

Last

(eds) Tracking Environmental Change Using Lake Sediments, Volume 3, Terrestrial, Algal, and Siliceus Indicators. Dordrecht; London: Kluwer Academic Publishers, pp. 99–119.

62.

Van Geel

Aptroot

(2006) Fossil ascomycetes in Quaternary deposits. Nova Hedwigia 82: 313–329.

63.

Van Geel

Coope

van der Hammen

(1989) Palaeoecology and stratigraphy of the Lateglacial type section at Usselo (The Netherlands). Review of Palaeobotany and Palynology 60: 25–129.

64.

Van Geel

Hallewas

Pals

(1983) A late Holocene deposit under the Westfriese Zeedijk near Enkhuizen (Prov. of N-Holland, The Netherlands): Palaeoecological and archaeological aspects. Review of Palaeobotany and Palynology 38: 269–335.

65.

Van Geel

Buurman

Brinkkemper

. (2003) Environmental reconstruction of a Roman Period settlement site in Uitgeest (The Netherlands), with special reference to coprophilous fungi. Journal of Archaeological Science 30: 873–883.

66.

Van Geel

Gelorini

Lyaruu

. (2011) Diversity and ecology of tropical African fungal spores from a 25,000-year palaeoenvironmental record in southeastern Kenya. Review of Palaeobotany and Palynology 164: 174–190.

67.

Van Geel

Mur

Ralsa-Jasiewiczowa

. (1994) Fossil akinetes of Aphanizomenon and Anabaena as indicators for medieval phosphate-eutrophication of Lake Gosciaz (Central Poland). Review of Palaeobotany and Palynology 83: 97–105.

68.

Vegas-Vilarrúbia

Rull

Montoya

. (2011) Quaternary palaeoecology and nature conservation: A general review with examples from the neotropics. Quaternary Science Reviews 30: 2361–2388.

69.

Vigo

(2005) Les comunitats vegetals: descripció i classificació. Barcelona: Universitat de Barcelona.

70.

Walker

(2001) Midges: Chironomidae and related Diptera. In: Smol

Birks

JHB

Last

(eds) Tracking Environmental Change Using Lake Sediments, Volume 4, Zoological Indicators. Dordrecht; London: Kluwer Academic Publishers, pp. 43–66.

71.

Weckström

Yliniemi

. (2009) The ecology of Pediastrum (Chlorophyceae) in subarctic lakes and their potential as paleobioindicators. Journal of Paleolimnology 43: 61–73.

72.

Wilmshurst

McGlone

(2005) Origin of pollen and spores in surface lake sediments: Comparison of modern palynomorph assemblages in moss cushions, surface soils and surface lake sediments. Review of Palaeobotany and Palynology 136: 1–15.