- Original Article
- Open Access
Microscopic species make the diversity: a checklist of marine flora and fauna around the Island of Sylt in the North Sea
- Werner Armonies1Email authorView ORCID ID profile,
- Harald Asmus1View ORCID ID profile,
- Christian Buschbaum1View ORCID ID profile,
- Dagmar Lackschewitz1,
- Karsten Reise1View ORCID ID profile and
- Johannes Rick1View ORCID ID profile
- Received: 7 December 2017
- Accepted: 20 June 2018
- Published: 26 June 2018
Abstract
Based on the past 150 years of research and ongoing time-series observations we give a comprehensive overview of marine species composition around the island of Sylt in the eastern North Sea. A total of 2758 species is listed according to the categories microplankton (591 species), zooplankton (137), nekton (118), benthic microflora (158), benthic macroflora (125), benthic micro-and meiofauna (1204), benthic macrofauna (509), birds and mammals (91), and neobiota (39). Plants account for a third of the species, most (85%) of them are microscopic Chromista. Among animals, 60% of the species are micro- and meiofauna though this faunal component is still insufficiently known. These figures are similar to records from the southern North Sea and therefore may by typical for temperate climate sedimentary coastal areas. A comparison with the total of marine species suggests that the small benthic fauna may be severely understudied over most of the world. Analysis of global change depends on sound baseline data and species inventories like this can assist in the detection of biodiversity changes. They emphasise rare species and the full range of local habitats while time-series measurements usually rely on a few selected habitats and biotic components to generate a very general picture of the state of an ecosystem.
Keywords
- Marine biodiversity
- Species inventory
- Long-term ecological research
Background
Biological research has a long tradition in the North Sea and especially around the German island of Sylt in the north-Frisian Wadden Sea. Here, Möbius [1] began with studies on the associated species community of oyster beds in the middle of the nineteenth century. In 1924 the Biologische Anstalt Helgoland founded an oyster laboratory in the village of List on Sylt, which has developed over the decades to the current Wadden Sea Station Sylt, belonging to the Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research (German: Wattenmeerstation Sylt, Alfred-Wegener-Institut Helmholtz-Zentrum für Polar- und Meeresforschung). In the first half of the previous century, benthic research was continued by Hagmeier and Kändler [2]. Additionally, Nienburg [3] described the vegetation and Wohlenberg [4] the tidal flat benthos of Königshafen, the bay adjacent to the Wadden Sea Station at the northern tip of the island of Sylt, where most field research has been conducted and student courses studied and still investigate the biology of coastal organisms. Künne was the first to devote a study to the regional plankton [5].
Several studies in the coastal ecosystem have repeated surveys from early in the twentieth century 50–80 years later to reveal temporal change [e.g. 6, 7]. During recent decades, regular observations were initiated which are still carried on. All these studies together with numerous contributions by guest scientists of the Wadden Sea Station Sylt provided the sources for the lists of species compiled for the sea around the island of Sylt. Although there are still gaps—not all taxa have yet been studied or listed—this is an exceptionally comprehensive compilation of species found in a coastal sea. More than 150 years of research have contributed to this treasure of marine biological science. Facing enhanced global warming and biological globalization as well as local human pressure, this regional assessment of species richness will be of outstanding value for understanding and then hopefully managing the rapid change in coastal biodiversity.
Methods
Position of the studied area in the North Sea
For species names we used the World Register of Marine Species (http://www.marinespecies.org) as a reference [10], only few species were not yet included in WoRMS. The latest update of the species names in our lists was in March 2018; changes of species names at a later date can be examined by following the link to WoRMS given with each species. Each taxon list was compiled and checked by an expert in the respective group of organisms to ensure data quality.
Results
- (1)
Microplankton—Additional file 1: Table S1
The microplankton check list results from a long-term time series initiated by Gerhard Drebes and Malte Elbrächter who have sampled and analysed net plankton from Sylt-Rømø Bight from the early seventies. In 1987 the protocol was standardized and is now known as the semi-quantitative Sylt Roads time series [47] consisting of weekly samples (20 and 80 µm nets) from a fixed station (Fig. 1; 55.03°N, 008.46°E). Evaluation of the live material starts < 1 h after sample collection and includes an inspection with a dissection microscope followed by an intense analysis (90 min) with a Leitz Aristoplan microscope using seawater immersion lenses 25 and 50× with final magnification of 250× and 500×.
- (2)
Zooplankton—Additional file 1: Table S2
Starting from a basic study by Hickel [13], Peter Martens initiated a long-term time series on Zooplankton in Sylt-Rømø bight in 1975 which is still continued. The zooplankton species list is based on these data, completed with data on bivalve larvae [14] and gelatinous zooplankton [15].
- (4)
Benthic microflora—Additional file 1: Table S4
The microphytobenthos checklist is a taxonomically updated version of earlier unpublished compilations by Asmus on diatoms, and Hoppenrath on dinoflagellates and Euglenophyceae.
- (5)
Benthic macroflora—Additional file 1: Table S5
A high number of macroalgal species occurring around the island of Sylt have already been described in Kornmann and Sahling [22]. Twenty years later, Schories et al. [23] gave a first comprehensive overview on macroalgae species in the area. The present list of species is based on this compilation, expanded by published original papers and unpublished Ms. and Ph.D. theses dealing with macroalgae. In addition, the herbal material available at Wadden Sea Station Sylt was evaluated.
- (6)
Benthic Micro- and Meiofauna—Additional file 1: Table S6
In 2002 and 2003, Gerlach compiled a checklist of micro- and meiofauna in the Wadden Sea of Schleswig–Holstein and Denmark [24] including detailed references for each species. Since there were no major studies on local meiofauna in the meantime, only some 20 species have been added which means minor change in a list of some 1200 species. However, advanced methods in taxonomy led to major changes in systematics. As a result, some 160 of the species have been re-named since 2004. Additional file 1: Table S6 is an update of Gerlach [24] including these changes.
- (7)
Benthic Macrofauna—Additional file 1: Table S7
This species inventory is based on an internal list of macrobenthic species in the Northern Wadden Sea compiled by Christian Buschbaum and Karsten Reise in the year 2002, covering the published data as well as unpublished Ms. and Ph.D. theses until the year 2000. This list was expanded to include the North Sea off Sylt down to some 30 m depth and updated with respect to current species names. However, most data come from small-sized sediment samples (box or Van Veen cores); therefore, large sized benthos (megafauna) is not adequately represented in this listing.
- (8)
Birds and mammals—Additional file 1: Table S8
A first species inventory for birds and mammals was compiled by Birgit Hussel in 2002 and included terrestrial species recorded at the island of Sylt. Recent updates of this list also consider the reference material in Berndt [25] and Koop and Berndt [26, 27] and recent new findings in the online portal www.ornitho.de. In addition, the list was updated using monitoring data along the coast of the island of Sylt provided by Landesamt für Küstenschutz und Nationalpark des Landes Schleswig- Holstein (birds) and quantitative data provided by Institut für Terrestrische und Aquatische Wildtierforschung, Stiftung der Tierärztlichen Hochschule Hannover in Büsum and the Fiskeri- og Sjøfartsmuseet, Esbjerg (mammals) and from literature sources of master and doctoral theses.
Neobiota includes non-indigenous species (NIS) and cryptogenic species (for which we have no firm proof that they are introduced). Our list is based on data from ‘Rapid Assessment Surveys (RAS)’ for monitoring alien species in German coastal waters, conducted annually since 2009 and funded by state and federal authorities. In addition, investigations performed during Ms. and Ph.D. theses at Wadden Sea Station Sylt were evaluated. This revealed several species new for Sylt and ten species new for the entire German coast.
Major data sources: Buschbaum et al. [29], Lackschewitz et al. [30], Lackschewitz and Buschbaum [31], Nehring and Leuchs [32] and Reise et al. [33].
Discussion
Taxonomic species composition of flora and fauna around the Island of Sylt in the North Sea
No of species | Table | |
---|---|---|
Bacteria | ||
Cyanophyceae | 1 | 1.11 |
Protozoa | ||
Amoebozoa | 3 | 1.01 |
Choanozoa | 9 | 1.08 |
Euglenozoa | 49 | 1.13, 4.03 |
Incertae sedis | 7 | 1.16 |
Chromista | ||
Hacrobia | ||
Cryptophyta | 7 | 1.10 |
Haptophyta | 19 | 1.03 |
Heliozoa | 1 | 1.14 |
Alveolata | ||
Ciliophora | 123 | 6.02 |
Dinophyceae | 263 | 1.02, 4.02 |
Heterokonta | ||
Bigyra Bicosoecia | 2 | 1.06 |
Bacillariophyceae | 278 | 1.01, 4.01 |
Phaeophyceae | 39 | 5.02 |
Dictyochophyceae | 7 | 1.12 |
Raphidophyceae | 7 | 1.17 |
Xanthophyceae | 1 | 1.21 |
Oomycota | 10 | 1.15, 1.09 |
Rhizaria | ||
Cercozoa | 6 | 1.18 |
Foraminifera | 7 | 6.01 |
Radiozoa | 2 | 1.04, 1.20 |
Plantae | ||
Chlorophyta | 62 | 1.07, 5.01 |
Fucophyceae | 39 | 5.02 |
Rhodophyta | 38 | 5.03, 1.19 |
Tracheophyta | 8 | 5.04 |
Animalia | ||
Porifera | 3 | 7.01 |
Cnidaria | 47 | 2.01, 7.02, 6.03 |
Ctenophora | 5 | 2.02 |
Echinodermata | 12 | 2.08, 7.18 |
Xenacoelomorpha | 65 | 6.04 |
Platyhelminthes | 337 | 2.10, 6.05 |
Nemertea | 8 | 7.04, 6.07 |
Gastrotricha | 60 | 6.09 |
Gnathostomulida | 10 | 6.06 |
Rotifera | 30 | 6.08 |
Nematoda | 321 | 6.10 |
Kinorhyncha | 2 | 6.11 |
Mollusca | ||
Bivalvia | 65 | 2.04, 7.07 |
Polyplacophora | 1 | 2.03, 7.05 |
Gastropoda | 38 | 7.06 |
Annelida | ||
Polychaeta | 152 | 2.05, 6.12, 7.08 |
Oligochaeta | 46 | 7.09, 6.13 |
Arthropoda | ||
Chelicerata | ||
Acari | 28 | 6.15 |
Pycnogonida | 6 | 7.17 |
Crustacea | ||
Ostracoda | 22 | 6.16 |
Cirripedia | 6 | 7.11 |
Copepoda | 146 | 6.17, 2.07 |
Phyllopoda | 3 | 2.07 |
Amphipoda | 88 | 7.10, 3.01 |
Cumacea | 17 | 7.12 |
Decapoda | 26 | 7.13, 3.01 |
Isopoda | 8 | 7.14 |
Mysida | 12 | 7.15, 3.1 |
Tanaidacea | 1 | 7.16 |
Tardigrada | 3 | 6.14 |
Insecta | 3 | 7.21 |
Bryozoa | 14 | 2.11, 7.03 |
Phoronida | 2 | 7.22 |
Sipuncula | 1 | 7.23 |
Chaetognatha | 2 | 2.06 |
Hemichordata | 1 | 7.19 |
Chordata | ||
Tunicata | 10 | 2.9, 7.20 |
Pisces | 78 | 3.2, 7.24 |
Aves | 88 | 8.1 |
Mammalia | 3 | 8.2 |
Total species | 2758 |
Species richness along the coastlines of Belgium (southern North Sea) and the island of Sylt (eastern North Sea)
Sylt | Belgium | |
---|---|---|
Protozoa | 68 | na |
Chromista | 772 | na |
Plantae | 143 | 131 |
Animalia, total | 1772 | 2056 |
Macrofauna, predominantly sessile | 23 | 217 |
Porifera | 3 | 34 |
Cirripedia | 6 | 27 |
Bryozoa | 14 | 156 |
Macrofauna, predominantly mobile | 678 | 886 |
Polychaetaa | 152 | 152 |
Mollusca | 104 | 129 |
Pisces | 78 | 127 |
Aves | 88 | 75 |
Amphipoda | 88 | 71 |
Decapoda | 26 | 72 |
Cnidaria | 47 | 55 |
Isopoda | 8 | 33 |
Echinodermata | 12 | 27 |
Cumacea | 17 | 13 |
Mysida | 12 | 18 |
Tunicata | 10 | 11 |
Nemerteaa | 8 | 12 |
other macrofaunal taxa | 28 | 93 |
Meiofauna | 1071 | 953 |
Nematoda | 322 | 473 |
Platyhelminthesb | 337 | 161 |
Copepoda | 146 | 194 |
Ostracoda | 22 | 56 |
Gastrotricha | 60 | 36 |
Xenacoelomorpha | 65 | 0 |
Oligochaetab | 46 | 11 |
Rotifera | 30 | 20 |
Acari | 28 | 0 |
Gnathostomulida | 10 | 0 |
Kinorhyncha | 2 | 2 |
Tardigrada | 3 | 0 |
Phytoplankton is not included in the Belgian data but we found a comparable phytoplankton checklist for the sea off Roscoff (France) close to the southern border of the North Sea [35]. They report on 211 phytoplankton species (including 152 species of diatoms and 42 of dinoflagellates) which is only a third of the Sylt number. Again, this may be due to lower sampling intensity (10 years with 200 samples near Roscoff versus 30 years with > 1400 samples near Sylt) and the local availability of taxonomic expertise. Most (85%) of the Roscoff species also occur near Sylt indicating the phytoplankton species spectrum may be rather similar all over the North Sea. The remaining 15% of phytoplankton species found near Roscoff but not near Sylt are predominantly Lusitanian or Atlantic species as expected from the geographical position of Roscoff.
On a world-wide scale the number of species recorded from Sylt (2758) roughly equals 1% of the number of marine species described (some 240,000) [10], and 8% of the species recorded from European waters (some 33,500) [36]. Again, there are strong variations over taxonomic units (Additional file 1: Table S12). Reasons for low representation of taxa in the eastern North Sea include a lack of local studies as in Bacteria and Fungi, habitat effects such as the local lack of hard substrata (e.g., Porifera, Bryozoa, macroalgae, with effects on the associated fauna), and geographical restrictions in some taxa. On the other hand, in the North Sea some faunal taxa include exceptionally high percentages of the world-wide known species. This may be due to wide geographic ranges of the species brought about by wide physiological tolerance and/or high mobility of species as in birds. For other taxa such as Xenacoelomorpha, Platyhelminthes, Gastrotricha, Gnathostomulida, and Rotifera the exceptional high study intensity in the North Sea is a likely cause. But since there are no reasons why meiofaunal species richness should by higher in the North Sea than along other coastlines of the world, these high percentages indicate that small fauna is severely understudied over most of the world. As a consequence, without adequate registration of the small flora and fauna marine diversity is likely to be strongly underestimated.
Limitations of the compiled species lists
Despite the wealth of species recorded from Sylt our compilations are not complete but species richness of major taxa is biased by varying study intensity. This explains the high species numbers for many meiofaunal taxa that were intensively studied in the 1970s [37] as well as the low species number for bacteria and fungi that have not been studied at all in the sea surrounding the island of Sylt, up to now. In addition, habitats have not been equally studied. As an example, though a high number of meiofaunal species has been listed, most of them were recorded from inter- or supratidal habitats while nearly nothing is known about their counterparts living in the subtidal. Since these organisms may dominate benthic species richness from the shallows [38] to the deep sea [39] the lack of studies in the subtidal part of our study area results in an underestimate of micro- and meiofaunal species richness.
Phytoplankton species richness in the Sylt Roads time series. Mean number of species per weekly sample ± standard error for entire years (annual mean) and single seasons. The R2 in spring refers to a linear regression and the arrows indicate low values after strong ice winters
Finally, man-made translocations of species (intentional or accidentally) contribute to changes in species richness. Currently, the number of non-indigenous species still seems low (39 out of 2758 equivalent to 1.4%) but some of the introduced species already had fundamental effects on the communities [41]. Examples are American razor clams Ensis leei which became a dominant bivalve in terms of abundance and biomass in the subtidal zone of the Wadden Sea [42], Pacific oysters Magallana (Crassostrea) gigas which turned the former mussel (Mytilus edulis) beds into combined oyster/mussel beds [43, 44], or the Japanese seaweed Sargassum muticum which forms extensive beds in the shallow subtidal zone and nowadays functionally replaces former native seagrass (Zostera marina) beds that almost went extinct in the 1930s due to a parasitic slime mould [45] and failed to recover to their original extension, up to now. Most of the non-indigenous species recorded so far are either planktonic or large benthic species. Presumably, this is an artefact brought about by study intensity which is highest for planktonic and macrobenthic communities while for small-sized micro- and meiofauna low sampling intensity meets insufficient knowledge of the species thus preventing non-indigenous species to be recognized. Our species inventory intends to reduce this bias.
Benefits of species checklists
Local species checklists may be a useful tool to assist students in species identification. They provide regional baseline data to detect natural diversity developments and the impact of local anthropogenic pressures, hence provide a data source for management measures and decisions [46]. Nevertheless, comprehensive species inventories like ours are extremely scarce, on a world-wide scale. The reasons for this rarity certainly include the large effort needed to compile the data. More important, however, may be the need for taxonomic experts for the various taxa. Therefore a checklist usually can only be compiled (or updated) by treating taxa one-by-one, as an expert is available, and it may take decades until all taxa are included.
Despite their rarity, comprehensive checklists may fundamentally contribute to analysis of global change. Since long-term ecological research and time-series measurements are usually cost-limited they need to concentrate on a few selected habitats and biotic components. This may yield excellent data on some abundant species and may be used as a proxy for the general state of an ecosystem but fails to detect change in rare species and all the components not included in the time-series. Updated species inventories are highly useful to fill that gap.
Declarations
Authors’ contributions
All authors contributed to both the text and Additional file 1. All authors read and approved the final manuscript.
Acknowledgements
None.
Competing interests
The authors declare that they have no competing interests.
Availability of data and materials
The datasets generated during the current study are available in Additional file 1. Major datasets used during the current study are listed in ‘Data sets’.
Ethics approval and consent to participate
Not applicable. This article does not contain any studies with animals performed by any of the authors.
Funding
This study was completely funded by our home institute—no third-party funding.
Publisher’s Note
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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
Authors’ Affiliations
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