Biological richness of a large urban cemetery in Berlin. Results of a multi-taxon approach

Abstract Background Urban green spaces can harbor a considerable species richness of plants and animals. A few studies on single species groups indicate important habitat functions of cemeteries, but this land use type is clearly understudied compared to parks. Such data are important as they (i) illustrate habitat functions of a specific, but ubiquitous urban land-use type and (ii) may serve as a basis for management approaches. New information We sampled different groups of plants and animals in the Weißensee Jewish Cemetery in Berlin (WJC) which is one of the largest Jewish cemeteries in Europe. With a total of 608 species of plants and animals, this first multi-taxon survey revealed a considerable biological richness in the WJC. In all, 363 wild-growing vascular plant, 72 lichen and 26 bryophyte taxa were recorded. The sampling also yielded 34 bird and 5 bat species as well as 39 ground beetle, 5 harvestman and 64 spider species. Some species are new records for Berlin.


Introduction
Cities can harbor a considerable number of plant and animal species (McKinney 2008, Shwartz et al. 2014. While there is a great deal of information on the biological richness of urban forest remnants and parks (e.g. Croci et al. 2008, Nielsen et al. 2014, cemeteries are clearly understudied, although this land-use type is ubiquitous in cities all over the world. Cemeteries are important components of the urban green infrastructure, simply because of their number and the area they cover. Berlin, for example, has 220 cemeteries within its limits, with a total area of about 1,125 hectares (SenStadtUm 2014).
A few studies on plants and animals, summarized in textbooks by Klausnitzer 1993 andSukopp 1990 illustrate that cemeteries within a large city may play an important role for urban biodiversity due to their size, habitat heterogeneity and habitat continuity. Yet similarly to biodiversity studies on urban parks in general (Nielsen et al. 2014), earlier studies on the flora or fauna of cemeteries in Berlin have focused on single species groups and rarely comprise flora and fauna.
The present paper provides the first comprehensive inventory of a large urban cemetery in Berlin, the Weißensee Jewish cemetery (WJC), which is also one of the largest Jewish cemeteries (if not the largest) in Europe (Rütenik et al. 2013). The data set resulting from our multi-taxon approach includes information about the occurrences of several groups of plant taxa (vascular plants, bryophytes, lichens) and animal taxa (bats, birds, ground beetles, harvestmen, spiders). These data were recorded to support a World Heritage Initiative beginning in 2006, in particular to illustrate habitat functions of WJC that may back future approaches in linking biodiversity conservation and heritage preservation (Kowarik et al. 2011, Rütenik et al. 2013).

Study site
The study was performed in Berlin, Germany, which has a population of 3.5 million people within an area of 892 km . The WJC is 39.2 ha and is situated in northeastern Berlin (central point: 52°32'40"N, 13°27'30"E). It was established in 1880 by the Jewish community and has about 116,000 graves (Rütenik et al. 2013). The design and plant use at WJC is similar to that of contemporary Christian cemeteries, with cemetery sections separated by tree-lined avenues (von der Lippe et al. 2011). The cemetery was never destroyed, but the numbers of burials and the intensity of management sharply declined at the end of the 1930s due to the Shoah (Rütenik et al. 2013). As a consequence, large parts of the WJC developed into woodland (Figs 1, 2). While only smaller parts of WJC, close to the entrance, were covered with frequently mowed lawns or with intensively managed ornamental plantings, major parts are dominated by trees. These woodlands are subject to different management intensities, ranging from regularly managed parts to unmanaged parts where wild woodlands were allowed to develop (Figs 1, 2). The main focus of management efforts is on uprooting wild tree saplings and shrubs. Vegetation structure and prevailing plant species are similar to other spontaneously grown woodlands in Central European cemeteries, with Acer platanoides, A. pseudoplatanus and Fraxinus excelsior as dominant tree species, and Hedera helix, Dryopteris filix-mas and Impatiens parviflora as abundant herb species (Passarge 1990). Features of the sepulchral architecture (types, materials, age), which shape many habitats for mosses, lichens and vascular plants, are extensively reported by Rütenik et al. 2013.

Sampling methods
We sampled different groups of plants and animals in a nested design on three spatial scales (Table 1): an area-wide recording of the entire cemetery for bats, birds and vascular plants; a sampling of selected cemetery sections (n= 30) and selected family graves for lichens and bryophytes; and a sampling of 10 x 10 m plots (one in each of 30 selected cemetery section) for vascular plants, carabid beetles, harvestmen and spiders.

Identification methods & analyses
For the multi-taxon survey, field observations and samplings were done by five experts (  Table 2). Ground-dwelling arthropods caught in the traps were identified by three experts in the laboratory.

Data resources
In all, 363 wild-growing vascular plant taxa were recorded. Of these, 140 grew within the sample plots (Table 3). Twenty-five plant taxa were of conservation concern (Fig. 3): 15 Table 2.
Identification methods and experts of taxa sampled in the Weißensee Jewish Cemetery. Experts: AL = Andreas Lemke, AS = Axel Schönhofer, BS = Birgit Seitz, JS = Jens Scharon, KH = Karsten Hannig, TB = Theo Blick, TT = Tobias Teige, VO = Volker Otte species were threatened, 5 species were near-threatened and 3 species, Centaurium erythraea, Epipactis helleborine and Helichrysum arenarium, were protected by law. Two species, Potentilla sterilis and Urtica subinermis were newly recorded for Berlin. Urtica subinermis was formerly assessed as a subspecies of Urtica dioica (Buttler and Hand 2007). The sampling of 30 cemetery sections revealed 72 taxa of lichens and 27 taxa of bryophytes (Tables 4, 5, Fig. 5). Two bryophytes and five lichens were threatened, one lichen species (Hyperphyscia adglutinata) was considered to be extinct in Berlin and one ( Aloxyria ochrocheila) was newly recorded for Berlin and is very rare in northeastern Germany.
The area-wide recording yielded 34 bird and 5 bat species (Tables 6, 7). All bat species are listed in Annex IV of the Flora-Fauna-Habitat Directive and are thus of special conservation concern. Furthermore, nine of the bird species are protected (Fig. 4).  Examples for species with conservation concern: the lichen Aloxyria ochrocheila. Photo: V. Otte.  Dysderidae Dysdera crocata 10 * 3

Harpactea rubicunda
All species were native to Berlin except 118 species of vascular plants. The differentiation of natives and neophytes (post-1492 introductions) followed Seitz et al. 2012. Native species and pre-1492 introductions (i.e., archeophytes) were not differentiated.

Conclusion
Our dataset illustrates that old cemeteries within a large city can harbor a considerable biological richness and therefore may play an important role for urban biodiversity conservation. Our results add evidence to findings from urban cemeteries and urban parks with large woodland patches (e.g., Graf 1986, Fudali 2001, Kocian et al. 2003, Croci et al. 2008, Gao et al. 2013, Philpott et al. 2014), but, for the first time, from a multi-taxon perspective. Our sampling approaches yield an overview over species assemblages of a range of groups of taxa. Yet due to limited sampling pressure, the inventories of the ground-dwelling arthropods are likely incomplete. Accordingly, species richness estimators show that a higher diversity can be expected, for example by applying other sampling techniques and catching for a larger timespan. However, although a two month sampling period is rather short, recent studies have shown that this period is sufficient to yield reliable data (Pearce et al. 2004, Vergnes et al. 2014. Pitfall traps only catch surface running species while species occurring in higher vegetation strata are rarely caught (Jimenez-Valverde and Lobo 2005). So further hand-sampling or sweep-netting studies should add a number of web building species to the species inventory presented. Since conservation and environmental planning is often restricted to few taxa (Gobbi et al. 2012), our dataset is especially important as it is the first which provides evidence that urban cemeteries could have an overall positive habitat function for many groups of taxa. Our data is thus a valuable snapshot that illustrates the relevance of this large urban cemetery for biodiversity conservation in Berlin. This is important information for urban planners, conservationists and gardeners that, however, needs being substantiated by further studies on the role of cultural parameters (e.g., management intensity) and environmental parameters (e.g., vegetation structure) in modulating biodiversity functions for different groups of taxa.