Philippa Kaur

Molecular Phylogeny of Paramecium bursaria and Identification of its EndosymbiontsThe SSU and ITS rDNA of the nuclear ribosomal operon were sequenced to infer the genetic variability of the investigated strains. The SSU and ITS rDNA sequences were aligned according to their secondary structure (examples are presented for the strain SAG 27.96; Fig. 1 and Supplementary Fig. 1). Additional sequences acquired from GenBank were incorporated into a dataset, which included all syngens also from references known for P. bursaria. The phylogenetic analyses revealed five highly supported lineages among the P. bursaria strains, which corresponded to their syngen assignment. As demonstrated in Fig. 2, all investigated strains belonging to the syngens R1, R2 and R5 originated from Europe, whereas the others of the syngens R3-R4 showed a worldwide distribution. The three known green algal endosymbionts, i.e., Chlorella variabilis (Cvar), Chlorella vulgaris (Cvul) and Micractinium conductrix (Mcon) showed no or only little affiliation to specific syngens.Figure 1ITS‐1 (A) and ITS-2 (B) secondary structures of Paramecium protobursaria, SAG 27.96 (syngen R1).Full size imageFigure 2Molecular phylogeny of the Paramecium bursaria species complex based on SSU and ITS rDNA sequence comparisons. The phylogenetic tree shown was inferred using the maximum likelihood method based on the datasets (2197 aligned positions of 19 taxa) using the computer program PAUP 4.0a169. For the analyses, the best model was calculated by PAUP 4.0a169. The setting of the best model was given as follows: TVM + I (base frequencies: A 0.2983, C 0.1840, G 0.2271, T 0.2906; rate matrix A–C 2.6501, A–G 8.6851, A–U 5.3270, C–G 0.91732, C–U 8.6851, G–U 1.0000) with the proportion of invariable sites (I = 0.9544). The branches in bold are highly supported in all bootstrap analyses (bootstrap values  > 50% calculated with PAUP using the maximum likelihood, neighbour—joining, and maximum parsimony). The clades are named after the syngens (color‐coded) proposed by Greczek‐Stachura et al.10 and Bomford9 in brackets. The accession numbers are given after the strain numbers. The endosymbiotic green algae identified are highlighted (Mcon—Micractinium conductrix, Cvar—Chlorella variabilis and Cvul—Chlorella vulgaris) after the origin of the P. bursaria strains. The reference strain of each syngen is marked with an asterisk. The strains used for morphological comparisons are marked with a green dot next to the strain number.Full size imageSynapomorphies of the Paramecium bursaria SyngensAs demonstrated in Fig. 2, the subdivision of the P. bursaria strains into syngens is supported by the phylogenetic analyses of the SSU and ITS rDNA sequences. To figure out if these splits were also supported by characteristic molecular signatures, we studied the secondary structures of both SSU and ITS of all available sequences. We discovered 30, respectively 23 variable positions among the SSU and ITS sequences (numbers of these positions in the respective alignments are given in Fig. 3). All syngens showed characteristic patterns among the SSU and ITS. Only the syngens R1 and R2 could not be distinguished using the SSU only, however, in combination with the ITS, each syngen is characterized by unique synapomorphies as highlighted in yellow (Fig. 3). In addition, few variable base positions within syngens (marked in blue in Fig. 3) have been recognized in the ITS regions. For comparison with literature data, we also analyzed all available sequences of the mitochondrial COI gene to find synapomorphies for the five syngens. Within this gene, only 18 variable positions at the amino acid level could be discovered of which 13 are diagnostic for the five syngens (Fig. 3).Figure 3Variable base positions among the SSU, ITS rRNA, and COI sequences of the five syngens among the Paramecium bursaria species complex. The unique synapomorphies are highlighted in yellow, variable positions marked in blue.Full size imageThe synapomorphies discovered above were used to get insights into the geographical distribution of each P. bursaria syngen. Despite the complete SSU and ITS rDNA sequences included in the phylogeny presented in Fig. 2, records of the partial SSU or ITS rDNA sequences are available in GenBank (BLASTn search; 100% identity;13). Considering the metadata of our investigated strains and of the entries in GenBank (Supplementary Table 1), we constructed three haplotype networks using the Templeton-Crandall-Sing (TCS) approach. The SSU haplotype network (Fig. 4) containing 84 records showed that the syngens R1, R2 and R5 were only found in Europe, whereas the other three syngens have been discovered around the world. A similar distribution pattern occurred when using the ITS (101 entries in GenBank). Records of syngens R1 and R5 have only been found in Europe, whereas all other syngens were distributed around the world. The 132 COI records found in GenBank by the BLASTn search were used for the haplotype network, which also showed the similar pattern (Fig. 4).Figure 4TCS haplotype networks of the five syngens inferred from SSU, ITS rRNA, and COI sequences of the Paramecium bursaria species complex. This network was inferred using the algorithm described by Clement et al.40,41. Sequence nodes corresponding to samples collected from different geographical regions.Full size imageCiliate TaxonomyConsidering all our findings, P. bursaria is morphologically highly variable, and obviously represents a cryptic species complex (Figs. 5, 6; Supplementary Table 2). The known five syngens most likely represent biological species according to Mayr14 and can be attributed to the cryptic species described by Greczek-Stachura et al.11. As mentioned above, the assignments of these cryptic species by Greczek-Stachura et al.11 have not been validly described according to the ICZN. In addition, the naming using a mixture of Latin prefix and Greek suffix is also not appropriate (the epithet bursa derived from the Greek word byrsa). Therefore, we describe the five syngens as new species as follows. The general morphological features of these species are summarized in Table 1.Figure 5Ventral views of Paramecium bursaria morphotypes in vivo: P. protobursaria (syngen R1), i.e., strains SAG 2645 (A) and PB-25 (B); P. deuterobursaria (syngen R2), i.e., strains CCAP 1660/36 (C) and CCAP 1660/34 (D); P. tritobursaria (syngen R3), i.e., strains CCAP 1660/28 (E), CCAP 1660/26 (F) and CCAP 1660/31 (G); P. tetratobursaria (syngen R4), i.e., strains CCAP 1660/25 (H) and CCAP 1660/33 (I); P. pentobursaria (syngen R5), i.e., strain CCAP 1660/30 (J). Scale bar 20 µm.Full size imageFigure 6Morphological details of the Paramecium bursaria species complex from specimens of strains PB-25 (A), CCAP 1660/30 (B), SAG 2645 (C, F, G, I, L–N), CCAP 1660/36 (D), CCAP 1660/26 (E, H), CCAP 1660/30 (J, O), CCAP 1660/16 (K) in vivo (A–F, H–O) and after silver nitrate staining (G). Adoral membranelles (A, B), endosymbiotic algae Micractinium conductrix (C), caudal and somatic cilia (D), arrows denote excretory pores of the contractile vacuoles: extruded extrusomes are shown and caudal cilia (E), ventral views showing the preoral suture and the oral opening (F), the ciliary pattern (G), arrows denote excretory pores of the contractile vacuoles (H), trichocysts and symbiotic algae underneath the pellicula (I, J), cell size variations (K), radial collecting channels (white arrows) and excretory pores (black arrows) of contractile vacuoles (L), macro- and micronucleus (M), cytopyge and characteristic rectangular pellicular pattern (N), pattern of the pellicula (O). AS anterior suture, CC caudal cilia, CP cytopyge (cell after), CV contractile vacuole, EP excretory pore of a contractile vacuole, EX extrusomes, M1–M3 membranelles 1–3, MA macronucleus, MI micronucleus, OO oral opening, S symbiotic algae, SC somatic cilia, SK somatic kineties, UM undulating membrane. Scale bars 10 µm (A, I), 20 µm (B, D–H, J, L–O), 50 µm (K).Full size imageTable 1 Main morphometric and morphological characteristics of the Paramecium bursaria syngens (min and max values).Full size table
Paramecium protobursaria sp. nov.Synonym: Paramecium primabursaria nom. inval.Description: The strains SAG 27.96 and PB-25 belong to syngen R1 according to Greczek-Stachura et al.10,11 and differ from other syngens by their SSU and ITS rDNA sequences (MT231333). From morphology, the cells are ellipsoidal to broadly ellipsoidal and dorso-ventrally flattened in vivo. The cells measure 70–164 × 44–65 µm; the single macronucleus is located around mid-cell and measures 25–38 × 11–22 µm; the adjacent single compact micronucleus measures 11–20 × 5–8 µm; the usually two (rarely one) contractile vacuoles, one in the anterior and one in the posterior cell portion have radial collecting channels and 1–3 excretory pores each; the number of ciliary rows/20 µm is 14–22; the length of the caudal cilia is 9–19 µm; the numerous trichocysts located in the cell cortex are 4–6 µm in length. The symbiotic algae belong to M. conductrix; the larger algae measure 4–7 × 4–7 µm; the smaller algal cells measure 2–5 × 2–5 µm.Geographic distribution: The investigated strains of syngen R1 were found in Europe: Göttingen, Germany; Lake Mondsee, Austria. In addition, this species has been reported from different places in Europe, Asia and North America (see details in Supplementary Table 1).Reference material: Strain SAG 27.96 and the clonal strain SAG 2645 derived from SAG 27.96 are available at the Culture Collection of Algae (SAG), University of Göttingen, Germany.Holotype: Two slides (one holotype, one paratype) with protargol-impregnated specimens from the clonal culture SAG 2645, which derived from the reference material SAG 27.96, isolated from the pond of the Old Botanical Garden of the University of Göttingen (Germany), have been deposited in the Oberösterreichisches Landesmuseum at Linz (LI, Austria).Zoobank Registration LSID: AFD967ED-BC2A-43FD-847E-5DF588BB025C.
Paramecium deuterobursaria sp. nov.Synonym: Paramecium bibursaria nom. inval.Description: The strains CCAP 1660/34 and CCAP 1660/36 belong to syngen R2 according to Greczek-Stachura et al.10,11 and differ from other syngens by their SSU and ITS rDNA sequences (OK318487). From morphology, the cells are ellipsoidal to broadly ellipsoidal and dorso-ventrally flattened in vivo. The cells measure 81–167 × 35–83 µm; the single macronucleus is located around mid-cell and measures 24–46 × 10–32 µm; the adjacent single compact micronucleus measures 10–18 × 5–9 µm, no micronucleus seen in live cells of strain CCAP 1660/34; the usually two (rarely one or three) contractile vacuoles, one in the anterior and one in the posterior cell portion have radial collecting channels and 1–3 excretory pores each; the number of ciliary rows/20 µm is 13–22; the length of the caudal cilia is 11–20 µm; the numerous trichocysts located in the cell cortex are 4–6 µm in length. The symbiotic algae belong to M. conductrix; the larger algae measure 5–7 × 4–7 µm; the smaller algal cells measure 3–5 × 2–5 µm.Geographic distribution: The investigated strains of syngen R2 were found in Europe: Zurich, Switzerland; Lake Piburg, Austria. In addition, this species has been reported from different places in Europe, Asia and Australia (see details in Supplementary Table 1).Reference material: Strain CCAP 1660/36 is available at the Culture Collection of Algae and Protozoa (CCAP) at the Scottish Association for Marine Science, Oban, Scotland.Holotype: Two slides (one holotype, one paratype) with protargol-impregnated specimens from the reference material CCAP 1660/36, isolated from Lake Piburg (Tyrol, Austria), have been deposited in the Oberösterreichisches Landesmuseum at Linz (LI, Austria).Zoobank Registration LSID: D1C20BE6-9A15-4A3D-A7E5-DFC31FF04679.
Paramecium tritobursaria sp. nov.Synonym: Paramecium tribursaria nom. inval.Description: The strains CCAP 1660/26, CCAP 1660/28 and CCAP 1660/31 belong to syngen R3 according to Greczek-Stachura et al.10,11 and differ from other syngens by their SSU and ITS rDNA sequences (MT231339). From morphology, the cells are ellipsoidal to broadly ellipsoidal and dorso-ventrally flattened in vivo. The cells measure 80–153 × 49–73 µm; the single macronucleus is located around mid-cell and measures 21–53 × 12–31 µm; the adjacent single compact micronucleus measures 9–17 × 3–6 µm; no micronucleus seen in live cells of strain CCAP 1660/28; the usually two (rarely one or three) contractile vacuoles, one in the anterior and one in the posterior cell portion have radial collecting channels and 1–3 excretory pores each; the number of ciliary rows/20 µm is 12–20; the length of the caudal cilia is 8–19 µm; the numerous trichocysts located in the cell cortex are 4–6 µm in length. The symbiotic algae belong to C. variabilis; the larger algae measure 4–7 × 3–6 µm; the smaller algal cells measure 3–5 × 2–4 µm.Geographic distribution: The investigated strains of syngen R3 were found in Europe and Asia: Lake Piburg, Austria; Tokyo, Japan; Khabarovsk region, Amur River, Russia. In addition, this species has been reported from different places in Europe, Asia, North and South America as well as in Australia (see details in Supplementary Table 1).Reference material: Strain CCAP 1660/26 is available at the Culture Collection of Algae and Protozoa (CCAP) at the Scottish Association for Marine Science, Oban, Scotland.Holotype: Two slides (one holotype, one paratype) with protargol-impregnated specimens from the reference material CCAP 1660/26, isolated from Japan, have been deposited in the Oberösterreichisches Landesmuseum at Linz (LI, Austria).Zoobank Registration LSID: CC0FBA7E-9E3A-4C37-B424-C9BFF2018EC0.
Paramecium tetratobursaria sp. nov.Synonym: Paramecium tetrabursaria nom. inval.Description: The strains CCAP 1660/25 and CCAP 1660/33 belong to syngen R4 according to Greczek-Stachura et al.10,11 and differ from other syngens by their SSU and ITS rDNA sequences (MT231347). From morphology, the cells are ellipsoidal to broadly ellipsoidal and dorso-ventrally flattened in vivo. The cells measure 65–179 × 37–79 µm; the single macronucleus is located around mid-cell and measures 18–53 × 10–29 µm; the adjacent single compact micronucleus measures 8–18 × 4–10 µm; the usually two (rarely one or three) contractile vacuoles, one in the anterior and one in the posterior cell portion have radial collecting channels and 1–3 excretory pores each; the number of ciliary rows/20 µm is 14–19; the length of the caudal cilia is 12–20 µm; the numerous trichocysts located in the cell cortex are 4–7 µm in length. The symbiotic algae belong to C. variabilis (CCAP 1660/25) and M. conductrix (CCAP 1660/33); the larger algae measure 3–6 × 3–6 µm; the smaller algal cells measure 2–5 × 1–4 µm.Geographic distribution: The investigated strains of syngen R4 are found in North- and South America: Burlington, North Carolina, USA; San Pedro de la Paz, Laguna Grande, Chile. In addition, this species has been reported from Europe (see details in Supplementary Table 1).Reference material: Strain CCAP 1660/25 is available at the Culture Collection of Algae and Protozoa (CCAP) at the Scottish Association for Marine Science, Oban, Scotland.Holotype: Two slides (one holotype, one paratype) with protargol-impregnated specimens from the reference material CCAP 1660/25, isolated from a pond in Burlington (North Carolina, USA), have been deposited in the Oberösterreichisches Landesmuseum at Linz (LI, Austria).Zoobank Registration LSID: 78BA9923-07A9-4918-AD7C-9E5E15CC9CDB.
Paramecium pentobursaria sp. nov.Synonym: Paramecium pentabursaria nom. inval.Description: The strain CCAP 1660/30 belongs to syngen R5 according to Greczek-Stachura et al.10,11 and differs from other syngens by their SSU and ITS rDNA sequences (MT231348). From morphology, the cells are ellipsoidal to broadly ellipsoidal and dorso-ventrally flattened in vivo. The cells measure 161–194 × 76–99 µm; the single macronucleus is located around mid-cell and measures 24–47 × 19–31 µm; the adjacent single compact micronucleus measures 13–20 × 4–9 µm; the usually two (rarely one or three) contractile vacuoles, one in the anterior and one in the posterior cell portion have radial collecting channels and 1–4 excretory pores each; the number of ciliary rows/20 µm is 13–19; the length of the caudal cilia is 14–25 µm; the numerous trichocysts located in the cell cortex are 5–7 µm in length. The symbiotic algae belong to C. variabilis; the larger algae measure 5–6 × 5–6 µm; the smaller algal cells measure 4–5 × 3–4 µm.Geographic distribution: The investigated strain of Syngen R5 was found in Europe: Astrakhan Nature Reserve, Russia.Reference material: Strain CCAP 1660/30 is available at the Culture Collection of Algae and Protozoa (CCAP) at the Scottish Association for Marine Science, Oban, Scotland.Holotype: Two slides (one holotype, one paratype) with protargol-impregnated specimens from the reference material CCAP 1660/30, isolated from Astrakhan Nature Reserve (Russia), have been deposited in the Oberösterreichisches Landesmuseum at Linz (LI, Austria).Zoobank Registration LSID: 6629FA71-E00F-48C6-83AB-61C0CA4823B6.Syngen Affiliation related to Ciliate Morphology, Endosymbionts and Geographic DistributionPearson-correlations of morphometric, syngen-specific and endosymbiont datasets of the P. bursaria strains revealed four significant positive correlations (p  r  > 0.75) between ciliate cell length (BLEN) and width (BWID), BWID and macronucleus width (MACWID), as well as length and width of large symbiotic algae (LSALEN and LSAWID; Fig. 7).Figure 7Pearson-correlations of morphometric, symbiont and syngen data of Paramecium strains under study. Colored dots indicate the strength of correlation, and the size of dots represent p-values. Bold squares highlight significant correlations, with − 0.75  > r  > 0.75 and p  1, accounting for 73.1% variation in total (Supplementary Table 3). Principal component axis 1 (PC1) appears to be most negatively weighted by syngen (SYN) and width of the macronucleus (MACWID), separating CCAP 1660/30 and CCAP 1660/33 from the other strains. Principal component axis 2 (PC2) is primarily positively influenced by symbiotic algae characteristics (LSALEN, LSAWID, small symbiotic algal length (SSALEN) and width (SSAWID)) and, ciliate cell length (BLEN) and width (BWID; Supplementary Table 4), partitioning strain PB-25, CCAP 1660/26 and CCAP 1660/36 from CCAP 1660/31 and SAG 27.96 (Fig. 8).Figure 8PCA of morphometric data of Paramecium bursaria strains. Only the top eight contributing variables are shown.Full size imageThe redundancy analysis (RDA; Fig. 9) revealed a large difference between morphometric features and the tested set of explanatory variables (i.e., algal species (ALSPEC), LSAWID, SSALEN, SYN and GEO) as only 26.9% of the total variation could be explained.Figure 9Ordination diagram for redundancy analysis (RDA) of morphometric data and shown syngen (SYN), geographic region (GEO), and algal features (ALSPEC, LSAWID and SSALEN) as explanatory features.Full size image More

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OverviewWe compiled systematically sampled empirical taxa occurrence across the landscape, and inferentially assembled respective blue and green local food webs by combining these data with a metaweb approach. We quantified key properties of the inferred food webs, then analysed with GIS-derived environmental information how focal food-web metrics change along elevation and among different land-use types in blue versus green systems. Details are given below.Assemble food webs using a metaweb approachWe applied a metaweb method to obtain the composition and structure of multiple local food webs across a landscape spatial scale10. A metaweb is an accumulation of all interactions (here, trophic relationships) among the focal taxa. In this study, we built our metaweb based on known trophic interactions derived from literature and published datasets, which themselves were all based on primary empirical natural history observations. We further complemented or refined the trophic interactions in the metaweb based on expert knowledge of primary observations that are not yet published or only accessible in grey literature. The expert knowledge covers authors and collaborators who have specific natural history knowledge on Central European plants, herbivorous insects, birds, fish, and aquatic invertebrates. Importantly, these observations were all based on empirical observations and/or unpublished data accumulated over considerable field research experience. The respective literature we referred, as well as the metaweb itself with information source of each trophic link (online repository), are provided in Supplementary Methods. By assuming that any interaction in the metaweb will realise if the interacting taxa co-occur, the metaweb approach allows an inference of local food webs if taxa occurrence is known. Such an assumption of fixed diets may lead to an over-estimation of the locally realised trophic links32, as it essentially ignores the possible intraspecific diet variation caused by resource availability61,62, predation risk63, temperature64, ontogenetic shift65, or other genetic and environmental sources66. Therefore, the food webs we inferred systematically using this method capture trophic relationships driven by community composition (species presence versus absence) but not the above-mentioned processes. Nonetheless, since the trophic interactions were based on empirical observations, the fixed diets can be seen as collapsing all intraspecific variations of diet-determining traits (or trait-matching) at species level, within which we know realisable interactions surely exist. This, together with co-occurrence as a pre-requisite, gives realistic boundaries for the potential interaction realisation, which is plausible and non-biased when applying to localised sites. With this approach, we were addressing a systematic comparison among potential local food webs between the blue and green systems and across the selected gradients. For sensitivity analyses considering the potential inaccuracy of the metaweb approach mentioned here, please see further below Food-web metrics and analyses and Supplementary Discussion.We compiled taxa occurrence of four terrestrial and two aquatic broad taxonomic groups (“focal groups”) to assemble local green and blue communities, respectively and independently, based on the well-resolved data available. Each focal group referred to a distinct taxonomic group, and the within- and among-group trophic relationships captured most of the realised interactions. These focal groups were vascular plants, butterflies, grasshoppers, and birds in the green biome, and stream invertebrates and fishes in the blue biome. Notably, with “butterflies” we refer to their larval stage and accordingly their mostly-herbivorous trophic interactions throughout this study. Larval interactions were also the predominant interaction assessed for stream invertebrates (i.e., all interactions of stream invertebrates focussed on their aquatic stage, which is predominant larval). The occurrence data of these focal groups were compiled from highly standardised multiple-year empirical surveys of various authorities, all conducted by trained biologists with fixed protocols (Supplementary Methods). The information across sites should thus be representative and can be up-scaled to the landscape. The occurrences of plants, butterflies, birds, and stream invertebrates were from the Biodiversity Monitoring Switzerland programme (BDM Coordination Office67) managed by the Swiss Federal Office for the Environment (BAFU/FOEN). The occurrences of grasshoppers and fishes were from the Swiss database on faunistic records, info fauna (CSCF), where we further complemented fish occurrence from the data of Progetto Fiumi Project (Eawag). In terms of biological resolution, taxa were resolved to species level in most cases, while the plant and butterfly groups included some multi-species complexes. Insects of the order Ephemeroptera, Plecoptera, and Trichoptera were resolved to species, while all other stream invertebrates were resolved to family level. These were each treated as a node later in our food-web assembly, and referred to as “species”, as the species within such complexes and families mostly share the same trophic role. Spatially, the occurrence datasets adopted coordinates resolved to 1 × 1 km2. The species that were recorded in the same 1 × 1 km2 grid were considered to co-occurred. We took the co-occurring four/two focal groups to form local green/blue local communities, respectively. To obtain better co-occurrence across group-specific data from different sources (e.g., BDM and info fauna), we intentionally coarsened the grasshopper and fish occurrence to 5 × 5 km2 coordinates. This is arguably a biologically acceptable approximation considering the high mobility of these two groups. Also, we only included known stream-borne fishes and dropped pure lake-borne ones to match our stream-only invertebrate occurrence data. Across all 462 green and 465 blue communities we assembled, we covered 2016 plant, 191 butterfly, 109 grasshopper, 155 bird, 248 stream invertebrate, and 78 stream fish species. Unlike the knowledge of plant occurrence in green communities, we did not have detailed occurrence information of the basal components (e.g., primary producers) in blue ones. Therefore, we assumed three mega nodes—namely plant (including all alive or dead plant materials), plankton (including zooplankton, phytoplankton, and other algae), and detritus—as the basal nodes occurring in all blue communities, without further discrimination of identities or biology within. These adding to our focal groups thus cover major taxonomic groups as well as trophic roles from producers to top consumers in both blue and green systems.Taking the above-assembled local communities then drawing trophic links among species (nodes) according to the metaweb yielded the local food webs (illustrated in Fig. 1), representatively covering the whole Swiss area. Notably, although our understanding of trophic interactions indeed encompassed some links across the blue and green taxa (e.g., between piscivorous birds and fishes), our occurrence datasets did not present sufficient spatial grids where these taxa co-occur. We, therefore, did not include such links, nor assembled blue-green interconnected food webs, but the blue and green food webs separately instead (but see Supplementary Discussion). Also, we dropped isolated nodes, i.e., basal nodes without any co-occurring consumer and consumer nodes without any co-occurring resource, from the inferred food webs. These could possibly be passing-by species that were recorded but had no trophic interaction locally, or those that interact with non-focal taxa whose occurrence information was unknown to us. We thus had to exclude them to focus on evidence-supported occurrences and trophic interactions. Nonetheless, across all cases, isolated nodes were rather rare (averaged less than 3% of species occurred in either blue or green communities).Environmental dataWe acquired environmental data across all of Switzerland (42,000 km2) on a 1 × 1 km2 grid basis (i.e., values are averaged over the grid) from GIS databases, with which we mapped environmental conditions to the grids where we assembled food webs. These included: topographical information from DHM25 (Swisstopo, FOT), land-cover information from CLC (EEA), and climate information (averaged over the decade of 2005–2015) from CHELSA. Among environmental variables, elevation and temperature are essentially highly correlated. In this study, we took elevation as the focal environmental gradient throughout, as after accounting for the main effects of elevation on temperature, the residual temperature was not a good predictor of the food-web metrics we looked at (see next section, and Supplementary Table 4). In other words, by analysing along the elevation gradient, we already captured most of the temperature influences on food webs. Based on the labels provided by the GIS databases, we categorised the originally detailed land cover into the five major land-use types that we used in this study, namely forest, scrubland, open space, farmland, and urban area. Forest includes broad-leaved, coniferous, and mixed forests. Scrub includes bushy and herbaceous vegetation, heathlands, and natural grasslands. Open space encompasses sparsely vegetated areas, such as dunes, bare rocks, glaciers and perpetual snow. Farmland include any form of arable, pastures, and agro-forestry areas. Finally, urban area is where artificial constructions and infrastructure prevail. As each grid could contain multiple land-use types, we then defined the dominant land-use type of the grid as any of the five above that occupied more than 50% of the grid’s area. Analyses separated by land-use types with subsetted food webs (land-use-specific analyses) were based on the grids’ dominant land-use type. There were a few grids where the dominant land-use type did not belong to the focal major five, e.g., wetlands or water bodies, and a few where no single land-use type covered more than 50% of the area. Food webs of these grids were still included in the overall analyses but excluded from any land-use-specific analyses (as revealed in the difference in sample sizes between all versus land-use type subsetted food webs in Fig. 2; analyses details below).Food-web metrics and analysesWe quantified five metrics as the measures of the food webs’ structural and ecological properties. For the fundamental structure of the food webs, the number of nodes (“No. Nodes”) reflects the size of the web, meanwhile represents local species richness (though the few isolated nodes were excluded as above-mentioned). Connectance is the proportion of realised links among all potential ones (thus bounded 0–1), reflecting how connected the web is. We also derived holistic topological measures, namely nestedness and modularity. Nestedness of a food web, on the one hand, describes the tendency that some nodes’ narrower diets being subsets of other’s broader diets. We adopted a recently developed UNODF index68 (bounded 0–1) that is especially suitable for quantifying such a feature in our unipartite food webs. On the other hand, modularity (bounded 0–1 with our index) reflects the tendency of a food web to form modules, where nodes are highly connected within but only loosely connected between. Nestedness and modularity are two commonly investigated structures in ecological networks and have been considered relevant to species feeding ecology24 and the stability of the system69. Finally, we measured the level of consumers’ diet niche overlap of the food webs (Horn’s index70, bounded 0–1), which essentially depends on the arrangement of trophic relationships (thus the structure of the webs), and could have strong ecological implications as niche partitioning has been recognised to be a key mechanism that drives species coexistence71,72. We selected these fundamental and holistic properties as they are potentially more relevant to the processes that may have shaped food webs across a landscape scale (e.g., community assembly), in comparison to some node- or link-centric properties. Also, addressing similar metrics as in the literature13,69 would facilitate potential cross-study comparison or validation.To first gain a glimpse of the structure of the blue and green food webs, we performed a principal component analysis (PCA; Fig. 3a) on the inferred food webs (n = 462 and 465 in green and blue, respectively) taking the four structural metrics (number of nodes, connectance, nestedness, and modularity) as the explaining variables of blue versus green system types. We then confirmed that system type, elevation, and land-use type were all important predictors of food-web metrics (whereas the residual temperature after accounting elevation effects was not) by conducting general linear model analyses, taking the former as interactive predictors while the latter response variables (Supplementary Tables 3, 4). To check how elevation influences food-web properties in blue and green systems separately, and how food-web properties depend on each other, we ran a series of piecewise structural equation modelling (SEM)73 analyses on inferred food webs (Fig. 3b, c) whose dominant land use can be defined (n = 421 and 430 in green and blue, respectively). This was also conducted on subsetted webs of each of the five major land-use types (Supplementary Figs. 1 and 2). The SEM relationships were derived from linear mixed model analyses with dominant land-use type as a random effect (assumption tests see Supplementary Figs. 12–17). The SEM structure of direct effects was set according to the literature13,69 and is illustrated in Fig. 3b. In short, this structure tests the dependencies from elevation (an environmental predictor) to food-web metrics (ecological responses). The further dependencies among food-web metrics themselves were assigned with the principle of pointing from relative lower-level properties to higher-level ones. That is, from number of nodes (purely determined by nodes) to connectance (determined by numbers of nodes and links), further to nestedness and modularity (holistic topologies, determined further by the arrangement of links), then to diet niche overlap (ecological functional outcome).Finally, to check and visualise the exact changing patterns of food webs, we applied generalised additive models (GAMs) to reveal the relationships between food-web metrics and the whole-ranged elevation (Figs. 4 and 5), as well as a particular comparison between food webs in forests and farmlands below 1500 m a.s.l. (Supplementary Fig. 5), as this elevation segment covered most of the sites belonged to these two land-use types. We also performed a series of linear models (LMs) and least-squared slope comparisons based on land-use-specific subsets of food webs (Figs. 4 and 5; Supplementary Figs. 3 and 4), to investigate whether food-web elevational patterns are different among land-use types (assumption tests see Supplementary Tables 5 and 6). In the GAMs analyses, specifically, we simulated two sets of randomised webs, i.e., “keep-group” and “fully”, as the null models to compare with the inferred ones74. Both randomisations generated ten independently simulated webs from each input inferred local food web, keeping the same number of nodes and connectance as of the latter. On the one hand, the keep-group randomisation shuffled trophic links from an input local web but only allowed them to realised fulfilling some pre-set within- and among-group relationships. That is, in green communities, birds can feed on all groups, grasshoppers on any groups but birds, while butterflies only on plants; in blue communities, fishes can feed on all groups, while invertebrates on themselves and the basal resources. These pre-set group-wide relationships captured the majority of realistic trophic interactions compiled in our metaweb. On the other hand, the fully randomised webs shuffled trophic links disregarding the biological identity of nodes. The GAMs of nestedness, modularity, and niche overlap illustrated the patterns of these randomised webs (Fig. 5). Comparing among the three types of webs, the patterns exhibited already by fully randomised webs should be those contributed by variations in web size and connectance, while the difference between keep-group and fully randomised webs by the focal-group composition of local communities, and the difference between inferred and keep-group randomised webs further by the realistic species-specific diets. In addition, we also applied the same GAMs and LMs approach to analyse node richness, as well as both realised and potential diet generality (vulnerability for plants) of each focal group (Supplementary Figs. 6–11). These analyses provided hints about the changes in community composition and species diet breadths along elevation and among land-use types, which helped explain the detected food-web responses in mechanistic ways.In addition, to check if our findings were shaped or strongly influenced by the potential inaccuracy of using the metaweb, we repeated the above PCA, SEM, and GAM analyses as a series of sensitivity analyses. We generated food webs based on our locally inferred ones (i.e., the observations) but with random 10% link removal. This procedure mimics the effect of potential intraspecific diet variation (mentioned earlier) so that some trophic interactions in the metaweb do not realise locally. Overall, these analyses with link removal showed that our conclusions are qualitatively and quantitatively highly robust, and only very minorly affected by the such potential inaccuracy of metawebs, which is also in accordance to other food-web studies (see e.g., Pearse & Altermatt 201575). All details and outcomes of these additional analyses are given in Supplementary discussion.All metric quantification and analyses were performed under R version 4.0.3 (R Core Team76). All applied packages and functions were described in Supplementary Methods, while the R scripts performing these tasks can be accessed at the online repository provided.Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

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We found a significant positive relationship between pollen- and plant richness regardless of differences in plant diversity, landscape structure and environmental conditions between the two study regions. This finding represents a major step stone towards more accurate paleoecological reconstructions of plant diversity in temperate Central Europe, as previous studies on this topic have mostly been conducted in boreal and boreal-nemoral zones8,11, in high mountain habitats10 or in southern Europe9,12.Methodological differences e.g., in diversity indices, data transformations or sample sizes used make comparison between studies difficult. Nevertheless, the strongest relationships seem to be found when habitats with contrasting patterns of plant diversity are compared, such as forests and alpine vegetation7 or forests, peatlands and grasslands11. Also in our study, we found the strongest correlations when complete datasets combining forested and open habitats were analysed together for both study regions. As it is well known that plant richness is generally lower in forests than in open landscapes across temperate and boreal regions28, this finding may seem rather trivial. However, it is important for paleoecological reconstruction because Holocene changes in diversity in temperate regions were largely driven by changes in the relative abundance of major habitat types (such as forests, grasslands, wetlands and man-made habitats), and not just by changes in species richness within these habitats5,6.Regarding individual habitats, the pollen-plant diversity relationship is often rather strong and significant in grasslands and other open habitats8,11; for example the WCM open-habitat subset in this study. Open habitats are generally richer in species, thus providing a longer gradient of species richness compensating for the taxonomical imprecision of the pollen analysis. In forested sites with less species, we found mostly non-significant relationships. Moreover, two other factors may play a role.First, high pollen productivity of trees biases the diversity relationship according to the studies from northern Europe16. However, a study from an elevational transect in southern Norway showed that the strongest bias in representation occurs only in the boreal forest biome, which is dominated by high pollen producers10. Our dominant vegetation component, Picea and Quercus, have intermediate to high pollen productivity (2–2.5), whereas true high pollen producers such as Alnus and Betula ( > 3) are less abundant in our study area (Supplementary Fig. S2). Adjustment of pollen counts by PPEs led to stronger relationship between pollen and floristic richness only in the WCM open-habitat subset (Supplementary Fig. S4).Second, interception of pollen by the tree canopies29 and subsequent washout to the forest floor affects the diversity relationship of forest sites more than pollen productivity. This noise described also as a vegetation filtering30 can be illustrated in our dataset by pollen of long-distance transport from Ambrosia artemisiifolia-type, which has the closest source populations ca. 50 km south-eastwards from WCM region31; or pollen of Artemisia, growing in open habitats. Both pollen taxa are more abundant in the forest than in open sites (Supplementary Fig. S3).Regarding the application of these results for the interpretation of fossil record, we suggest to consider only marked changes of pollen richness in the past and to avoid overinterpretation of small differences, as the non-significant relationships obtained in both forest datasets suggest some limitations of the method.We showed that the pollen-plant diversity relationship may be at least partly disentangled by knowing the exact spatial position of plant species in broader surroundings of the pollen sampling sites. Changes in the relationship with changing spatial scale are largely driven by the numbers of species newly appearing as the radius of surveyed area increases, especially as new habitats are added (Fig. 5, Supplementary Fig. S5). Remarkably, in the BMH region it increases with distance, whereas the opposite trend was observed in the WCM region. This discrepancy may be explained by non-uniform richness patterns in different habitats and by different landscape structure (i.e. spatial arrangement of different habitats) in the two study regions.At open-habitat sites in the WCM area, most species generally appeared within the first 40 m. This observation is consistent with the knowledge of extremely high fine-scale plant diversity in the local steppic meadows, where a substantial portion of the species pool occurs on a scale of tens of square meters32. Moreover, the grain size of the habitat mosaic in the WCM region is finer than in the BMH region. Therefore, the closest pollen-plant diversity relationship across habitats in the WCM region is achieved over shorter distances. Although habitats such as built-up areas and roads occurring at distances greater than 40 m may be species-rich and compositionally different from the grasslands and forests, it appears that high fine-scale plant diversity (in our case in WCM open-habitat subset) limits the influence of the surrounding landscape on pollen richness and reduces the source area of pollen richness. Several studies of the relevant source area of pollen report analogous results33,34,35. A weakening relationship between pollen diversity and plant diversity with distance has also been observed in the Mediterranean region9, although their interpretations are limited by field survey methodology.The appearance of open habitats within forests led to the increase of species numbers and the local maxima of adjusted R2 in both regions. While in the BMH forest the appearance of forest roads at about 70 m was crucial, meadows and orchards at about 250 m played a similar role in the WCM forest subset. In the WCM open-habitat subset diversity patterns in the first tens of metres were crucial, while in the BMH open-habitat subset increased correlation of floristic and pollen richness appeared only at 400 and 550 m; at this distance many species appeared due to the frequent transition of meadow complexes to shrubby habitats and built-up areas. Also other studies from semi-open landscapes found a high correlation between pollen richness and landscape openness17,26,27.Estimating the source area of pollen variance as a regression of pollen and floristic variance implies that the resulting distance of 100–250 m represents all datasets. Although they differ in species richness, openness and habitats, the relationship between variances is fairly linear. The exception is the WCM open-habitat subset suggesting that the spatial scale at which the pollen variance corresponds to the floristic variance cannot be generalized.The strong effect of high pollen richness in the WCM open-habitat subset is also visible in the comparison of pollen and floristic variance. At 150 m, the WCM open-habitat subset had much lower floristic variance than the other subsets. Floristic variance in this subset corresponding to the pollen variance and the pattern of the other datasets lay at 6 m (Fig. 6b). Again, this may be caused by the high fine-scale diversity of the meadows, which include most pollen types present in the surrounding landscape. Only a few new species appeared in broader surroundings and at 150 m, WCM open habitats are more similar than other analysed habitats. The fact that extremely high alpha diversity is compensated by low beta diversity has already been reported from the open habitats of the White Carpathians36. The linearity and the significance of the variance relationship within the rest of the datasets indicate robustness and possible applicability to a variety of fossil records.The mechanism of establishing the source area of pollen variance was similar to that mentioned for the source area of pollen richness. The appearance of new habitats with new species (Fig. 5) like open habitat for forest sites (WCM forest subset) or built-up areas for open sites (BMH open-habitat subset), caused small to negligible increases of floristic variance. Moreover, the high yet insignificant relationship of the variances at the distance between 250 and 600 m (Fig. 6a) corresponds to the distance of the second range of fit between floristic and pollen richness (Fig. 4a).Beta diversity, understood as directional turnover (temporal or spatial), is becoming more frequently used in pollen analysis22,24 than beta diversity as a non-directional variation. According to Nieto-Lugilde et al.25 pollen-based turnover correlates with forest-inventory-based turnover. We extend this finding from woody taxa to all species and from directional turnover to non-directional variance. Moreover, forest sites with high contributions to pollen beta diversity also show an increased contribution to floristic beta diversity (Fig. 4b).The reference data on plant diversity report 1477 species in 15 mapping squares covered by our survey for the BMH region and 2045 species in 14 squares for the WCM region37. It means that we recorded 54.1 and 53.7%, respectively, of the known regional species pool in the two regions. We consider this as a rather good result and the close agreement in representativeness between the two regions speaks for consistency in data quality between the datasets. We advise that future studies covering wider areas and various biomes should preferentially use high-quality floristic data collected in targeted field surveys rather than database data or data from simplified field surveys. Only then we will be able to understand the pollen-plant diversity relationships more realistically and in a spatially explicit manner.In order to interpret fossil pollen richness in the light of our present results, we need to consider landscape openness, which can be roughly inferred from the ratio of arboreal and non-arboreal pollen. Variation of pollen richness during the forest phases of the records should be interpreted more carefully, especially in cases of low variation. In all other cases, the pollen richness is significantly linked to the plant richness within a distance of ten to several hundreds of meters, depending on the distance of the expected species-rich patches. More

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