Although constituting more than 100,000 described species, protists are virtually ignored within the arena of biodiversity conservation. One reason is the widespread belief that the majority of protists have cosmopolitan distributions, in contrast to the highly hetereogenous biogeography of the “mega-Metazoa”. However, modern research reveals that about one third of the known protists have restricted distributions, which endorses their conservation, at least in special cases. Here, we report what probably ranks as the first successful conservation intervention focused directly on known protist diversity. It is justified by unique species, type localities, and landscape maintenance as evidence for legislation. The protected habitat comprises an ephemeral pond, which is now a “Natural Monument” for ciliated protozoa. This wetland occupies a natural depression on the Krauthügel (“cabbage hill”) south of the fortress of Salzburg City. When filled, the claviform pond has a size of ~30 × 15 m and a depth rarely surpassing 30 cm. Water is present only for some days or weeks, depending on heavy and/or prolonged rain. The pond occupied an agricultural field where root and leafy vegetables were cultivated for possibly more than 200 years. In the 1960s, this area became a grassland utilized as an autumn pasture, but was abandoned in the 1990s. Repeated sampling between 1982 and 2012 recovered a total of at least 150 ciliate taxa, of which 121 were identified to species level. Eight species were new to science, and an additional 10 poorly known species were reinvestigated and neotypified with populations from the Krauthügel pond. Both endemism and type localities justify the argument that the “integrative approach” in biodiversity and conservation issues should include protists and micro-metazoans. We argue that Krauthügel holds a unique reference node for biodiversity inventories to obtain the baseline knowledge—which is the prerequisite to monitor ecosystem integrity—and detect and evaluate impacts of natural and anthropogenic disturbances.
References
[1]
Finlay, B.J.; Corliss, J.O.; Esteban, G.; Fenchel, T. Biodiversity at the microbial level: the number of free-living ciliates in the biosphere. Q. Rev. Biol. 1996, 71, 221–237.
[2]
Finlay, B.J.; Esteban, G.F.; Fenchel, T. Protist diversity is different? Protist 2004, 155, 15–22, doi:10.1078/1434461000160.
[3]
Markert, B.A.; Breure, A.M.; Zechmeister, H.G. Bioindicators & Biomonitors Principles, Concepts and Applications; Elsevier: Amsterdam, the Netherlands, 2003; p. 997.
[4]
Cotterill, F.P.D.; Al-Rasheid, K.; Foissner, W. Conservation of protists: Is it needed at all? Biodivers. Conserv. 2008, 17, 427–443, doi:10.1007/s10531-007-9261-8.
[5]
Likens, G.E.; Lindenmayer, D.B. Integrating approaches leads to more effective conservation of biodiversity. Biodivers. Conserv. 2012, 21, 3323–3341, doi:10.1007/s10531-012-0364-5.
Fontaneto, D. Biogeography of Microscopic Organisms. Is Everything Small Everywhere?; Cambridge University Press: Cambridge, UK, 2011; p. 365.
[8]
Foissner, W. Protist diversity and distribution: Some basic considerations. Biodivers. Conserv. 2008, 17, 235–242, doi:10.1007/s10531-007-9248-5.
[9]
Cotterill, F.P.D.; Foissner, W. A pervasive denigration of natural history misconstrues how biodiversity inventories and taxonomy underpin scientific knowledge. Biodivers. Conserv. 2010, 19, 291–303, doi:10.1007/s10531-009-9721-4.
[10]
Parnell, J.; Hole, M.; Boyce, A.J.; Spinks, S.; Bowden, S. Heavy metal, sex and granites: Crustal differentiation and bioavailability in the mid-Proterozoic. Geology 2012, 40, 751–754, doi:10.1130/G33116.1.
[11]
Weisse, T.; Strüder-Kypke, C.; Berger, H.; Foissner, W. Genetic, morphological, and ecological diversity of spatially separated clones of Meseres corlissi Petz & Foissner, 1992 (Ciliophora, Spirotrichea). J. Eukaryot. Microbiol. 2008, 55, 257–270, doi:10.1111/j.1550-7408.2008.00330.x.
[12]
Foissner, W. Soil protozoa: fundamental problems, ecological significance, adaptations in ciliates and testaceans, bioindicators, and guide to the literature. Progr. Protistol. 1987, 2, 69–212.
[13]
Foissner, W. Basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. Europ. J. Protistol. 1991, 27, 313–330, doi:10.1016/S0932-4739(11)80248-8.
[14]
Perty, M. Zur Kenntniss kleinster Lebensformen nach Bau, Funktionen, Systematik, mit Specialverzeichnis der in der Schweiz beobachteten. Jent & Reinert: Bern, Switzerland, 1852; p. 228.
[15]
Foissner, W. Infraciliatur, Silberliniensystem und Biometrie einiger neuer und wenig bekannter terrestrischer, limnischer und mariner Ciliaten (Protozoa: Ciliophora) aus den Klassen Kinetofragminophora, Colpodea und Polyhymenophora. Stapfia 1984, 12, 1–165.
[16]
Kahl, A. Neue und erg？nzende Beobachtungen holotricher Infusorien. II. Arch. Protistenk. 1930, 70, 313–416.
[17]
Foissner, W.; Oertel, A. Morphology and ciliary pattern of some rare haptorid ciliates, with a description of the new family Kamburophryidae (Protists, Haptoria). Europ. J. Protistol. 2009, 45, 205–218, doi:10.1016/j.ejop.2008.11.002.
[18]
Dragesco, J. Revision du genre Dileptus., Dujardin 1871 (Ciliata Holotricha) (systématique, cytologie, biologie). Bull. Biol. Fr. Belg. 1963, 97, 103–145.
[19]
Vd’a？ny, P.; Foissner, W. Monograph of the dileptids (Protista, Ciliophora, Rhynchostomatia). Denisia 2012, 31, 1–529.
[20]
Stokes, A.C. Some new infusoria. Am. Nat. 1885, 19, 433–443.
[21]
Foissner, W. Neue und wenig bekannte hypotriche und colpodide Ciliaten (Protozoa: Ciliophora) aus B？den und Moosen. Zool. Beitr. N. F. 1987, 31, 187–282.
[22]
Müller, O.F. Vermium Terrestrium Et Fluviatilium, Seu Animalium Infusorium, Helminthicorum Et Testaceorum, Non Marinorum, Succincta Historia. Heineck & Faber: Havniae, Denmark & Lipsiae, Germany, 1773; p. 135.
[23]
Stein, F. Charakteristik neuer Infusorien-Gattungen. Lotos 1859, 9, 2–5.
[24]
Golińska, K. Comparative studies on the morphology of Dileptus anatinus sp. n. (Holotricha, Gymnostomata). Acta. Protozool. 1971, 8, 367–378.
[25]
Kahl, A. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 1. Allgemeiner Teil und Prostomata. Tierwelt. Dtl. 1930, 18, 1–180.
[26]
Kahl, A. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 2. Holotricha au？er den im 1. Teil behandelten Prostomata. Tierwelt. Dtl. 1931, 21, 181–398.
[27]
Foissner, W.; Agatha, S.; Berger, H. Soil ciliates (Protozoa, Ciliophora) from Namibia (Southwest Africa), with emphasis on two contrasting environments, the Etosha region and the Namib Desert. Denisia 2002, 5, 1–1459.
[28]
Fabre-Domergue, P.L. Sur une nouvelle forme de colpode (Colpoda. henneguyi) et sur un flagellé pélagique. Annls. Microgr. 1889, 2, 351–357.
[29]
Foissner, W. Morphologie und Infraciliatur einiger neuer und wenig bekannter terrestrischer und limnischer Ciliaten (Protozoa, Ciliophora). Sber. Akad. Wiss. Wien. 1989, 196, 173–247.
[30]
Gabilondo, R.; Foissner, W. Four new fuscheriid soil ciliates (Ciliophora: Haptorida) from four biogeographic regions. Acta. Protozool. 2009, 48, 1–24.
[31]
Dujardin, F. Histoire Naturelle Des Zoophytes Infusoire; Suites à Buffon: Paris, France, 1841; p. 684.
[32]
Petz, W.; Foissner, W. Morphology and morphogenesis of Strobilidium. caudatum (Fromentel), Meseres corlissi n. sp., Halteria grandinella (Müller), and Strombidium rehwaldi n. sp., and a proposed phylogenetic system for oligotrichid ciliates (Protozoa, Ciliophora). J. Protozool. 1992, 39, 159–176.
[33]
Gelei, J. Die Marynidae der Sodagew？sser in der N？he von Szeged XIV Beitrag zur Ziliatenfauna Ungarns. Hidrol. K？zl. 1950, 30, 107–119, 157–158.
[34]
Foissner, W. Protozoenfauna. Volume 4/1: Colpodea (Ciliophora.); Fischer: Stuttgart, Germany, 1993; pp. I–X, 798.
[35]
Stein, F. Charakteristik neuer Infusorien-Gattungen. Lotos 1859, 9, 57–60.
[36]
Foissner, W. Morphologie und Taxonomie einiger neuer und wenig bekannter kinetofragminophorer Ciliaten (Protozoa: Ciliophora) aus alpinen B？den. Zool. Jb. Syst. 1981, 108, 264–297.
[37]
Xu, K.; Foissner, W. Descriptions of Protospathidium serpens (Kahl, 1930) and P. fraterculum n. sp. (Ciliophora, Haptoria), two species based on different resting cyst morphology. J. Eukaryot. Microbiol. 2005, 52, 298–309, doi:10.1111/j.1550-7408.2005.00046.x.
[38]
Foissner, W. ？kologische und systematische Studien über das Neuston alpiner Kleingew？sser, mit besonderer Berücksichtigung der Ciliaten. Int. Revue ges. Hydrobiol. 1979, 64, 99–140, doi:10.1002/iroh.19790640109.
[39]
Foissner, W. Taxonomie und ？kologie einiger Ciliaten (Protozoa, Ciliophora) des Saprobiensystems. II. Familie Chilodonellidae. Hydrobiologia 1988, 162, 21–45, doi:10.1007/BF00014331.
[40]
Berger, H.; Foissner, W. Morphology and biometry of some soil hypotrichs (Protozoa: Ciliophora). Zool. Jb. Syst. 1987, 114, 193–239.
[41]
Foissner, W. An updated compilation of world soil ciliates (Protozoa, Ciliophora), with ecological notes, new records, and descriptions of new species. Europ. J. Protistol. 1998, 34, 195–235, doi:10.1016/S0932-4739(98)80028-X.
[42]
Müller, O.F. Animalcula Infusoria Fluviatilia Et Marina, Quae Detexit, Systematice Descripsit Et Ad Vivum Delineari Curavit; N. M？lleri: Hauniae, Denmark, 1786; p. 367.
[43]
Foissner, W. Morphologie und Morphogenese von Psilotricha succisa (O.F. Müller, 1786) nov. comb. (Ciliophora, Hypotrichida). Protistologica 1983, 19, 479–493.
[44]
Foissner, W.; Hess, S.; Al-Rasheid, K.A.S. Two vicariant Semispathidium species from tropical Africa and central Europe: S. fraterculum nov. spec. and S. pulchrum nov. spec. (Ciliophora, Haptorida). Europ. J. Protistol. 2010, 46, 61–73, doi:10.1016/j.ejop.2009.09.002.
[45]
Gruber, A. Neue Infusorien. Z. Wiss. Zool. 1880, 33, 439–466.
[46]
Foissner, W.; Berger, H.; Blatterer, H.; Kohmann, F. Taxonomische und ？kologische Revision der Ciliaten des Saprobiensystems Band I–IV; Bayerisches Landesamtes für Wasserwirtschaft: Deggendorf, Germany, 1995; pp. 1–540.
[47]
Foissner, W.; Berger, H.; Schaumburg, J. Identification and Ecology of Limnetic Plankton Ciliates; Bayerisches Landesamtes für Wasserwirtschaft: Deggendorf, Germany, 1999; p. 793.
[48]
Oertel, A.; Wolf, K.; Al-Rasheid, K.; Foissner, W. Revision of the genus Coriplites Foissner, 1988 (Ciliophora: Haptorida), with description of Apocoriplites nov. gen. and three new species. Acta. Protozool. 2008, 47, 231–246.
[49]
Stadt Salzburg. Amtsblatt 2012, 4, 1–7.
[50]
Williams, D.D. The Biology of Temporary Waters; Oxford University Press: New York, NY, USA, 2006; p. 337.
[51]
Spandl, H. Die Tierwelt vorübergehender Gew？sser Mitteleuropas. Arch. Hydrobiol. 1926, 16, 74–132.
[52]
Gelei, J. über die Lebensgemeinschaft einiger tempor？rer Tümpel auf einer Bergwiese im B？rzs？nygebirge (Oberungarn) III Ciliaten. Acta. biol. hung. 1954, 5, 259–343.
[53]
Gelei, J. über die Lebensgemeinschaft einiger tempor？rer Tümpel auf einer Bergwiese im B？rzs？nygebirge (Oberungarn) I Die Tümpel. Acta. biol. hung. 1954, 5, 227–233.
[54]
Gelei, J.; Megyeri, J.; Szabados, M.; Varga, L. über die Lebensgemeinschaft einiger tempor？rer Tümpel auf einer Bergwiese im B？rzs？nygebirge (Oberungarn) VIII Allgemeine Betrachtungen. Acta. biol. hung. 1954, 5, 363–382.
Fenchel, T. The quantitative importance of the benthic microfauna of an arctic tundra pond. Hydrobiologia. 1975, 46, 445–464, doi:10.1007/BF00028286.
[57]
Foissner, W. Artenbestand und Struktur der Ciliatenz？nose in alpinen Kleingew？ssern (Hohe Tauern, ？sterreich). Arch. Protistenk. 1980, 123, 99–126, doi:10.1016/S0003-9365(80)80042-X.
[58]
Stout, J.D. The protozoan fauna of a seasonally inundated soil under grassland. Soil Biol. Biochem. 1984, 16, 121–125, doi:10.1016/0038-0717(84)90101-9.
[59]
Madoni, P. The contribution of ciliated protozoa to plankton and benthos biomass in a European ricefield. J. Eukaryot. Microbiol. 1996, 43, 193–198, doi:10.1111/j.1550-7408.1996.tb01390.x.
Bresslau, E. über Protozoen aus Rasenaufgüssen. Verh. dt. zool. Ges. 1922, 27, 88–90.
[62]
Foissner, W.; Kreutz, M. Systematic position and phylogenetic relationships of the genera Bursaridium, Paracondylostoma, Thylakidium, Bryometopus., and Bursaria. (Ciliophora: Colpodea). Acta Protozool. 1998, 37, 227–240.
ICZN (The International Commission on Zoological Nomenclature). International Code of Zoological Nomenclature; International Trust for Zoological Nomenclature: London, UK, 1999; p. 306.
[65]
Foissner, W.; Wenzel, F. Life and legacy of an outstanding ciliate taxonomist, Alfred Kahl (1877–1946), including a facsimile of his forgotten monograph from 1943. Acta. Protozool. 2004, 43 (Suppl.), 3–69.
Cotterill, F.P.D. The Second Alexandrian Tragedy, and the fundamental relationship between biological collections and scientific knowledge. In The Values and Valuation of Natural Science Collections, Proceedings of Conference at the Manchester Museum, Manchester, UK, 19–21 April 1995; Nudds, J.R., Pettitt, C.R., Eds.; Geological Society: London, UK; pp. 217–241.
[68]
Foissner, W. Neotypification of protists, especially ciliates (Protozoa, Ciliophora). Bull. Zool. Nom. 2002, 59, 165–169.
[69]
Wu, D.; Wu, M.; Halpern, A.; Rusch, D.B.; Yooseph, S.; Frazier, M.; Venter, J.C.; Eisen, J.A. Stalking the fourth domain in metagenomic data: searching for, discovering, and interpreting novel, deep branches in marker gene phylogenetic trees. PLoS One 2011, 6, e18011.
[70]
Hansen, A.J.; DeFries, R. Ecological mechanisms linking protected areas to surrounding lands. Ecol. Appl. 2007, 17, 974–988, doi:10.1890/05-1098.
[71]
Handelsman, J.; Rondon, M.R.; Brady, S.F.; Clardy, J.; Goodman, R.M. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 1998, 5, R245–R249, doi:10.1016/S1074-5521(98)90108-9.
[72]
Morgan, J.L.; Darling, A.E.; Eisen, J.A. Metagenomic sequencing of an in vitro-simulated microbial community. PLoS One 2010, 5, e10209, doi:10.1371/journal.pone.0010209.
[73]
Foissner, W.; Chao, A.; Katz, L.A. Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodivers. Conserv. 2008, 17, 345–363, doi:10.1007/s10531-007-9254-7.
Griffith, G.W. Do we need a global strategy for microbial conservation? Trends Ecol. Evol. 2012, 27, 1–2, doi:10.1016/j.tree.2011.10.002.
[76]
Mace, G.M. The role of taxonomy in species conservation. Phil. Trans. R. Soc. Lond. B. 2004, 359, 711–719, doi:10.1098/rstb.2003.1454.
[77]
Bernardo, J. A critical appraisal of the meaning and diagnosability of cryptic evolutionary diversity, and its implications for conservation in the face of climate change. In Climate Change, Ecology and Systematics; Hodkinson, T.R., Jones, M.B., Waldren, S., Parnell, J.A.N., Eds.; Cambridge University Press, The Systematics Association: Cambridge, UK, 2011; pp. 380–438.
