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No More Lake Balls (Aegagropila Linnaei Ku¨Tzing, Cladophorophyceae, Chlorophyta) in the Netherlands?

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No More Lake Balls (Aegagropila Linnaei Ku¨Tzing, Cladophorophyceae, Chlorophyta) in the Netherlands? Aquat Ecol (2009) 43:891–902 DOI 10.1007/s10452-009-9231-1 No more lake balls (Aegagropila linnaei Ku¨tzing, Cladophorophyceae, Chlorophyta) in The Netherlands? Christian Boedeker Æ Anne Immers Received: 30 May 2008 / Accepted: 6 January 2009 / Published online: 23 January 2009 Ó The Author(s) 2009. This article is published with open access at Springerlink.com Abstract Aegagropila linnaei, a freshwater green compared with different growth forms and habitats macroalga, had been abundant in several locations in from several other locations outside The Netherlands. The Netherlands before the 1960s. Both the ‘lake The sequences confirm the identity of the Dutch ball’ form of this alga and dense unattached mats material and indicate very little divergence both floating over the sediment have been described from between populations in different locations and these locations. After 1967, this species has not been between different growth forms. recorded anymore from The Netherlands. In 2007, several historical collection sites were surveyed for Keywords Cladophora aegagropila Á extant populations of A. linnaei. All habitats have Eutrophication Á Threatened freshwater algae Á changed drastically during the last 50 years and were Lake balls Á LSU rDNA Á Marimo Á affected severely by eutrophication. Populations of A. Molecular sequences Á Red list linnaei seem to have become extinct in all but one location (Boven Wijde, province Overijssel), where we found very small amounts of attached filaments. The attached form had not been reported previously Introduction from The Netherlands. Environmental conditions do not seem suitable anymore to maintain extensive The green macroalga Aegagropila linnaei Ku¨tzing unattached growth forms including the enigmatic (Cladophorophyceae) occurs in freshwater and some lake balls, and the species must be regarded as brackish environments and has essentially a palae- threatened in The Netherlands and we propose to arctic distribution (van den Hoek 1963; Pankow include A. linnaei in a national red list. The decline of 1965). The simple morphology consists of stiff, populations elsewhere is reviewed and discussed in branched uniseriate filaments and is very similar to this paper. In addition to morphological identification members of the related genus Cladophora Ku¨tzing. of the attached filaments, partial sequences of the A. linnaei is morphologically distinct from Clado- nuclear large subunit rDNA were generated and phora spp. by the lateral or subterminal, often opposite, sometimes serial insertion of branches; irregular cell shape and unrestricted insertion posi- C. Boedeker (&) Á A. Immers tions of branches especially in the basal parts; and National Herbarium of The Netherlands, Leiden development of rhizoids from the base of cells which University Branch, P.O. Box 9514, 2300 RA Leiden, The Netherlands can produce terminal haptera (van den Hoek 1963; e-mail: [email protected] Leliaert and Boedeker 2007; Soejima et al. 2008). 123 892 Aquat Ecol (2009) 43:891–902 The species is presumed to reproduce mainly or 1959), in the lake system Loosdrechtse Plassen in entirely vegetatively by means of fragmentation North Holland (Koster 1959), in Lake Zwarte Broek (Brand 1902; Acton 1916; van den Hoek 1963). in Friesland (Kops et al. 1911; Koster 1959), and in Based on morphological similarities, the species was several parts of the lake system ‘De Wieden’ in the placed in the genus Cladophora (as C. aegagropila province Overijssel (Koster 1959; Segal and Groen- (L.) Rabenhorst, van den Hoek 1963), but has hart 1967). Since then, Aegagropila balls or mats recently been recognized as its own monotypic genus have not been reported again, so the last record of this based on molecular evidence. It is placed in a species in The Netherlands is more than 40 years old. separate clade that is sister to the orders Siphonocla- Attached forms had never been reported from The dales and Cladophorales, together with several other Netherlands. species-poor, predominantly freshwater genera such Taking into account the long period during which as Arnoldiella, Basicladia, Pithophora and Wittrock- A. linnaei had not been recorded and the changes in iella (Hanyuda et al. 2002; Leliaert et al. 2003). the environment in the meantime, it was assumed Aegagropila linnaei can occur in several different that this species had disappeared from its original growth forms, depending on environmental condi- habitats. Therefore, the historical collection sites tions (Waern 1952; Sakai and Enomoto 1960; were visited to check whether this species and its Niiyama 1989). The species is best known for the characteristic ball-shaped growth form still might formation of spherical balls several centimeters in exist in The Netherlands. We further discuss the diameter, the so-called lake balls, marimo (in Japan), situation and threat to this species elsewhere. Partial or moss balls (in aquarium shops). These balls consist LSU rDNA sequences were generated to verify of many interwoven filaments. In Japan, the lake balls morphological identifications of putative material of are very popular and have been designated a ‘special A. linnaei and to investigate possible genetic natural monument’ (Kurogi 1980). The ball forms divergence between different growth forms, as well have also become very popular in the aquarium trade. as between populations from different habitats and The species can grow as unattached mats, floating locations. above the substrate in shallow water, or as attached epilithic or epizoic filaments. Different theories about the formation of the ball form have been proposed, Materials and methods but it is generally assumed that the formation is a mixture of mechanic processes through water motion Herbarium and literature survey of Dutch and features intrinsic to the species that help entan- locations glement, such as the stiff texture, the formation of rhizoids, and the growth pattern following the During a survey on the global distribution of A. abrasion of apical cells while rolling on the sediment linnaei based on herbarium specimens, it became (Wesenberg-Lund 1903; Acton 1916; van den Hoek obvious that there are very few recent collections of 1963; Kurogi 1980; Niiyama 1989; Einarsson et al. this species in general, with the majority of the 2004). It has been shown in culture experiments that herbarium specimens being more than 100 years old. stable balls can be produced when exposing loose For findings from The Netherlands that are neither filaments to a rolling motion (Nakazawa 1973). mentioned in available literature nor deposited in the A recent study from Japan also contributing to the collections of herbaria, we contacted several Dutch conservation of A. linnaei and the management of its organizations that carry out monitoring of aquatic habitats indicates the possibility of genetic differen- vegetation and/or water quality in different areas of tiation between different growth forms, and it The Netherlands. These include Stichting Natuurmo- emphasizes the necessity to extend conservation numenten, Stichting Floron, Landelijk Informatie- efforts to epilithic populations as well (Soejima centrum Kranswieren (LIK), Waternet, Waterschap et al. 2008). Reest and Wieden, and Wetterskip Fryslaˆn. Also Floating balls or unattached mats of A. linnaei several boat rental businesses and dive clubs in The have been found in several locations in The Nether- Netherlands were contacted for possible amateur lands: in Lake Naardermeer in North Holland (Koster sightings of ‘lake balls’. The locations in the resulting 123 Aquat Ecol (2009) 43:891–902 Table 1 Locations in The Netherlands where Aegagropila linnaei has been reported from, with information on reported growth forms and abundance of A. linnaei, the date of the last record, and sources Location (province) Lat. Long. Depth (m) Reported growth Notes on Last Herbarium Additional references forms of A. linnaei abundance record collectionsa 1. Naardermeer (North Holland) N52°1706000 E05°0701200 1 Unattached mats, balls Very abundant 1962 L, LD Koster (1959) 2. Wijde Blik (North Holland) N52°1301200 E05°0206000 1–2 Ball 1955 L 3. De Wieden (Overijssel) Beulaker Wijde N52°4200300 E06°0303600 1 Ball 1938 Koster (1959) Boven Wijde N52°4304800 E06°0603600 1 Tufts (herbarium), 1944 L ball (literature) Duinigermeer N52°4301200 E06°0000000 1 Ball 1967 Segal and Groenhart (1967) Zuideindigerwiede N5284203600 E0680404800 1 Balls 1951 L Segal and Groenhart (1967) Molengat N52°4402400 E6°0502400 1–(3) Unattached mats Numerous; 1960 L, LD Segal and Groenhart (1967), dense masses van den Hoek (1963) 4. Zwarte Broek and N53°1500000 E05°5602400 1 Unattached tufts, balls Not common, 1906 BI, BR, BRNU, Kops et al. (1911) nearby ditches (Friesland) but numerous L, NY, PC The location numbers correspond to Fig. 1 a Herbarium acronyms follow Holmgren et al. (1990) 123 893 894 Aquat Ecol (2009) 43:891–902 stones. Shore observations were concentrated to areas with reed stands and leeward bays or shores. Material resembling A. linnaei was brought back to the laboratory and examined under a microscope. Veri- fied material of A. linnaei was vouchered and stored in L (the National Herbarium of The Netherlands, Leiden branch; see Table 3 for details). DNA sequence analysis Partial large subunit (LSU) rDNA sequences from six specimens of A. linnaei were analyzed to check the morphological identifications, covering different growth forms, habitats, and locations (including one Dutch site). Sample and collection information,
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