Discovery of the Rare Freshwater Brown Alga Pleurocladia Lacustris (Ectocarpales, Phaeophyceae) in California Streams

Western North American Naturalist

Volume 73 Number 2 Article 3

7-5-2013

Discovery of the rare freshwater brown alga Pleurocladia lacustris (Ectocarpales, Phaeophyceae) in California streams

John D. Wehr Fordham University, Armonk, NY, [email protected]

Rosalina Stancheva California State University, San Marcos, CA, [email protected]

Kam Truhn Fordham University, Armonk, NY, [email protected]

Robert G. Sheath California State University, San Marcos, CA, [email protected]

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Recommended Citation Wehr, John D.; Stancheva, Rosalina; Truhn, Kam; and Sheath, Robert G. (2013) "Discovery of the rare freshwater brown alga Pleurocladia lacustris (Ectocarpales, Phaeophyceae) in California streams," Western North American Naturalist: Vol. 73 : No. 2 , Article 3. Available at: https://scholarsarchive.byu.edu/wnan/vol73/iss2/3

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Western North American Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Western North American Naturalist 73(2), © 2013, pp. 148–157

DISCOVERY OF THE RARE FRESHWATER BROWN ALGA PLEUROCLADIA LACUSTRIS (ECTOCARPALES, PHAEOPHYCEAE) IN CALIFORNIA STREAMS

John D. Wehr1,3, Rosalina Stancheva2, Kam Truhn1, and Robert G. Sheath2

ABSTRACT.—Pleurocladia lacustris A. Braun is a freshwater member of the Phaeophyceae, a class of algae that occurs almost entirely in marine waters. It has previously been reported from only about 13 freshwater locations worldwide, just 2 of which are in North America. Outside of North America, P. lacustris has been listed as a threatened species on several European red lists. In this paper, we report the discovery of P. lacustris in 3 calcareous streams draining the Santa Lucia Mountains in coastal California, sites that are more than 1200 km from the nearest known population. Pleu- rocladia lacustris is a filamentous, benthic species that forms distinctive hemispherical colonies. It co-occurs with the green alga Cladophora glomerata and species of cyanobacteria (Rivularia, Nostoc, Schizothrix spp.). Detailed color illus- trations of the diagnostic macroscopic and microscopic features are provided and appear identical to those features of European populations. In the California streams, P. lacustris and other associated algae co-precipitate CaCO3 to form carbonate crusts on rocks. Preliminary ecological data are consistent with other streams and lakes in Europe where P. lacustris has also been reported (pH > 8.0, calcareous substrata, travertine). The global distribution of this presumed rare alga is also described and examined with respect to a specialized ecological niche.

RESUMEN.—Pleurocladia lacustris A. Braun es un organismo de agua dulce perteneciente a Phaeophyceae, una clase de algas que habita casi exclusivamente aguas marinas. Ha sido reportada solo en aproximadamente trece sitios de agua dulce en todo el mundo y sólo dos sitios en los Estados Unidos. Fuera de Norteamérica, está incluida en varias listas rojas de Europa como especie amenazada. En este trabajo presentamos el hallazgo de P. lacustris en 3 arroyos con material calcáreo que confluyen en las Montañas de Santa Lucía en la costa de California y se encuentran a más de 1200 km de la población conocida más cercana. Es una especie filamentosa, bentónica, que forma colonias hemisféricas distinti- vas y coexiste con el alga verde Cladophora glomerata y especies de cianobacterias (Rivularia, Nostoc, Schizothrix spp.). Mostramos ilustraciones detalladas en color de las características macroscópicas y microscópicas, donde se puede apre- ciar que son idénticas a las poblaciones europeas. En los arroyos de California, P. lacustris y otras algas asociadas precip- itan CaCO3 y forman cortezas de carbono sobre las rocas. La información ecológica preliminar coincide con la de otros arroyos y lagos de Europa donde se registró la presencia de esta alga (pH > 8.0, sustrato calcáreo, travertino). Además, se describe y se estudia la distribución global de esta alga aparentemente poco frecuente en relación con un nicho ecológico específico.

It has been hypothesized that due to their and is regarded as globally rare, possibly due small size, short generation time, and ease of to its close association with CaCO3 deposi - dispersal, microbial and algal taxa predomi- tion (travertine) in limestone springs (Pente- nantly have cosmopolitan distributions (Fenchel cost 1991, Rott et al. 2010). In recent years, and Finlay 2004, Vanormelingen et al. 2008). evidence has been growing that other fresh- But important exceptions exist. The well-rec- water algae have limited distributions. Several ognized freshwater green alga Aegagropila lin- are regional endemics with declining popula- naei Kützing is known on at least 3 continents, tions sufficient to receive conservation status yet it exists in disjunct locations and is declin- (Kilroy et al. 2007, Cotterill et al. 2008). The ing in number due to eutrophication and a factors leading to such declines are varied but very limited potential for dispersal (Boedeker include specialized ecological requirements et al. 2010). Other species of freshwater algae and loss of habitat, which can lead to further have very specific ecological requirements, isolated and rare taxa (Sherwood et al. 2004, making their biogeography similarly restricted. Coesel and Krienitz 2008). In other cases, The benthic desmid Oocardium stratum Nägeli, reports of algal endemism may be the result of a species known since 1849, is rarely observed either under-sampling or taxonomic confusion

1Louis Calder Center–Biological Field Station and Department of Biological Sciences, Fordham University, Armonk, NY 10504. 2Department of Biological Sciences, California State University, San Marcos, CA 92096. 3E-mail: [email protected]

148 2013] FRESHWATER PLEUROCLADIA IN CALIFORNIA 149

OR ID eral intermittently marine or brack ish locations (Eloranta et al. 2011). Some freshwater 1 NV UT populations have apparently been extirpated due to habitat degradation and urbanization CA (Sukopp 2003, Täuscher 2011, Wehr 2011), 1 Willow Creek ! AZ causing some European countries to list this species on their conservation red lists (Sie - mińska 2006, Täuscher 2010). In this paper, we report the recent discovery of P. lacustris Villa Creek in 3 streams in California. These streams con- ! stitute the fourth location for North America (third freshwater location), more than 1200 km from the nearest known population. We also Salmon Creek 1 ! examine the distribution of this species globally and discuss the presumed rarity of its occurrence (e.g., Siemińska 2006, Täuscher 2011). . 063 Kilometers STUDY AREA The study was conducted along the Big Sur coast in central California (Fig. 1). A previous collection of periphyton taken from a stream Fig. 1. Location of 3 stream populations of Pleurocladia lacustris (solid circles), with map of study area in west in this area on 23 June 2010 by the Surface central California (inset). Water Ambient Monitoring Program (SWAMP) of the California State Water Resources Control Board included material that was thought to (Whitford 1983, Vanormelingen et al. 2008). be P. lacustris. In the present study, we sur- The discovery of new populations of a pre- veyed 12 streams that drain the Santa Lucia sumed rare algal species may help to inform Mountains between Pfeiffer Big Sur State Park this discussion. and San Simeon, California. Most are first- or The Phaeophyceae is a large and diverse second-order streams and typically have very class of algae with roughly 270 genera and up - steep gradients with a calcareous geology (Hen - wards of 2000 taxa, of which more than 99% son and Usner 1993); CaCO3 precipitation occur in marine waters (Wehr 2003). They range and travertine formation are apparent at many in size from microscopic filaments to large locations. The region has a cool-Mediterranean kelps that form huge underwater for ests. The climate, and riparian vegetation is composed freshwater members of this class are modest mainly of white alder (Alnus rhombifolia ), big- in size, ranging from small filamentous tufts to leaf maple (Acer macrophyllum), arroyo willow pseudoparenchymatous crusts (united prostrate (Salix laseolepis), black cottonwood (Populus filaments), which may form macroscopically trichocarpa), California bay (Umbellularia cali- recognizable forms in streams and rivers (Kusel- fornica), and in some locations, coast redwood Fetzmann 1996). Few freshwater species are (Sequoia sempervirens). The streambed at most commonly observed. The crust-forming Herib- sites had variable canopy cover, with areas audiella fluviatilis (Areschoug) Svedelius is the ranging from open sun to heavy shade. Fur- most widely recognized spe cies, with a few ther details of the physical conditions of these hundred populations identified from many coun - streams are described by Rundio (2009). tries, although thus far only in the northern hemisphere (Wehr 2003). One of the lesser- METHODS known freshwater representatives is Pleuro- cladia lacustris A. Braun, a fila mentous species Stream sites were accessed from along a described more than 150 years ago (Braun 40-km stretch of California State Route 1, north 1855), yet observed only from few locations. from Cambria, California, 12–14 March 2012. Interestingly, P. lacustris has been reported All sampling reaches were located at least 150 from widely separated calcareous freshwater m upstream of any marine water. We collected environments (lakes and streams) and also sev- algae by using knives and razor blades to 150 WESTERN NORTH AMERICAN NATURALIST [Volume 73

TABLE 1. Locations and ecological conditions of California streams from which Pleurocladia lacustris was collected in 2012. Stream Salmon Creek Willow Creek Villa Creek Latitude (N) 35°48፱56.80፳ 35°53፱37.23፳ 35°50፱59.24፳ Longitude (W) 121°21፱31.82፳ 121°27፱40.71፳ 121°24፱28.23፳ Date 12 Mar 2012 12 Mar 2012 13 Mar 2012 Temperature (°C) 9.3 11.4 10.9 pH 8.22 8.45 8.50 Specific conductance (mS ⋅ cm−1) 220.9 253.2 271.2 sample rocks, and we inspected the material were not available, latitude and longitude val- with a Swift FM-31 field microscope. At sites ues for the names or nearest water body were where P. lacustris was present, samples were used. Geographic data for all populations were collected into bags or tubes (at least 10 repli- compiled and mapped using ArcGIS v. 10. cates per site) and separated for future use in mi crophotography, lab cultures, DNA extrac- RESULTS tion, and preserved samples. Live material was placed in sterile, 120-mL Whirl-Pak® bags Of 7 streams sampled, we located 3 that and stored on ice. Water temperature and spe- contained populations of Pleurocladia lacustris cific conductance were measured in situ by (Table 1). Water at all sites was alkaline (pH using a YSI EC300 meter, and pH was mea- >8.0) and had moderate specific conductance sured by using a YSI pH10A meter. A portable (average ~250 mS ⋅ cm–1). When present, this laboratory microscope (Nikon 50i with LED alga was among the most common and macro- illumination) was later used after each sam- scopically recognizable species in the stream. pling day to confirm identifications conducted Along with Pleurocladia, the filamentous green in the field. alga Cladophora glomerata and colonial cyano - Samples were shipped overnight to our bacteria Nostoc, Rivularia, and Schizothrix laboratories for further observations and mi - species were also common. Macroscopically, crophotography. In the laboratory, live algal the morphology of Pleurocladia appeared to samples were prepared for wet-mount micro - have 2 distinct forms: small irregular, flat scopy by using sterile probes to separate colo- brown spots on rocks (Fig 2A) and brown to nies prior to observation. Occasionally, dilute tan-colored hemispherical tufts (Fig. 2B). Both acid (1% HCl) was added to heavily calcified forms occurred in running water, but the colonies to improve clarity. Specimens were hemispherical form was more common in low- observed using a Nikon Eclipse E600 micro- current microhabitats, whereas the spreading scope with Nomarski (DIC) optics (200X, 400X, (flat-form) was more common in riffles. In the and 1000X total magnification), photographed field, colonies of both forms ranged in size using a Nikon DS-Fi1 digital camera, and from about 1 to 5 mm in diameter and ap- processed and measured using NIS-Elements peared dark brown or reddish brown in color. software. Identifications were based on Kusel- Where colonies were heavily calcified, they Fetzmann (1996), Wehr (2003), and Eloranta appeared light tan in color. Those that pro- et al. (2011). Georeferenced voucher specimens duced large quantities of elongate hyaline hairs were submitted to the William and Lynda (narrow, unpigmented filaments), grayish mats, Steere Herbarium at the New York Botanical or tufts were also apparent. Garden (NYBG), and DNA samples were Microscopically, basal filaments were all stored frozen (–40 °C) at the NYBG Molecular uniaxial and ranged in diameter from 12 to 20 Systematics Laboratory for a later study. Small mm, whereas upright filaments were 9–14 mm portions of live material were placed in algal wide (Figs. 2C–D). Branching frequency was growth media and maintained at Fordham irregular, although filaments in larger cush - University and the NYBG. ion-like colonies tended to be more elongate Past records of Pleurocladia lacustris were and have fewer side branches. In smaller or collected from published literature, personal younger colonies, the typical comb-like ap - communications with authors, and herbarium pearance was common. In both forms, cells in records. Where precise georeferenced records the main axes ranged from 10 to 35 mm in 2013] FRESHWATER PLEUROCLADIA IN CALIFORNIA 151

Fig. 2. Morphology of field populations of Pleurocladia lacustris from California streams: A, macroscopic appearance of dark brown, spreading (flat-form) colonies on rocks; B, macroscopic appearance of cushion-forming colonies (grayish material is a network of elongate hyaline cells); C, microscopic appearance of cushion-forming colonies with terminal hyaline cells (arrows); D, microscopic appearance of spreading colonies, with unilocular sporangia (arrows) and CaCO3 encrusting the colony base (brackets); E, detail of filaments with single parietal chloroplast and numerous oil bodies; F, detail of unilocular sporangium (left) on lateral side branch. 152 WESTERN NORTH AMERICAN NATURALIST [Volume 73

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Fig. 3. Geographic locations of all known populations of Pleurocladia lacustris (solid circles). Details of individual sites, including designations of freshwater, brackish, and marine locations, are given in the Appendix. length. Chloroplasts were single and parietal, 1200 km apart, but the macroscopic morphol- usually filling one-half to three-quarters of the ogy of the 2 populations is indistinguishable in cell diameter (Fig. 2E). In older cells, some terms of cell dimensions, branching pattern, chloroplasts appeared twisted or lobed. Nu- and sporangia. Both occur in calcareous river- merous spherical bodies, assumed to be oil ine habitats and commonly have CaCO3 en- droplets, were scattered throughout the cells. crusting at the base of the colonies (Fig. 2D). When present, terminal hyaline hair cells (Fig. One recent collection has also been made 2C) often would exceed 200 mm in length. from a deep limestone pool in South Australia Macroscopically, some appeared to extend more (deposited in the National Herbarium of New than 1 mm. Large, ovoid, or clavate unilocular South Wales; listed as Pleurocladia sp. nov. sporangia (20–40 × 30–85 mm) were frequently but without verification; #NSW 486949), a formed on short side branches (Fig. 2F). Pluri - site which is ~13,000 km from the California locular sporangia were not observed. populations and ~15,000 km from the nearest Following the discoveries in California, the freshwater population in Europe. global distribution of Pleurocladia lacustris now includes 8 countries, and 4 locations in DISCUSSION North America, totaling 27 separate freshwater stream or lake sites. Most sites are concen- The evidence for the existence of rare spe - trated in western and northern Europe (Fig. 3, cies of freshwater algae and other protists has Appendix), and many of these are located in been regarded somewhat skeptically by some eastern Sweden, including several rivers in researchers (Whitford 1983, Fenchel and Fin- the eastern Uppland province north of Stock- lay 2004). Reports of restricted distributions in holm and various standing waters in the Öre- freshwater algae may simply be the result of grund Archipelago area (Israelsson 1938, Waern undersampling (Foissner 2008). Some species 1952). Ecological information from these re - are seasonally ephemeral and missed by spot ports is spotty, but many researchers comment sampling. Others have cryptic life stages that on the calcareous nature of P. lacustris. Of all routine surveys may miss. However, studies the freshwater populations currently known, of freshwater algae in North America have the California sites are nearest to a population spanned more than 150 years, and certain spe - in the Green River, Utah, downstream of cies are still rarely seen. Evidence from multi- Flaming Gorge Dam (Ekenstam et al. 1996, ple studies in Europe suggest that there are Wehr 2003). These 2 locations are more than rare, threatened, and endangered species of 2013] FRESHWATER PLEUROCLADIA IN CALIFORNIA 153 algae that require conservation efforts (Brodie Guiral 1994, Aysel et al. 2008). The specific et al. 2007, Cotterill et al. 2008, Ros et al. conductance data from the 3 California sites 2009). This idea has been raised specifically (220–270 mS ⋅ cm–1) indicate that these popu- for Pleurocladia lacustris in the United King- lations have little or no marine influence. The dom, where the only known habitats have species is strictly benthic in habit but grows been altered through nutrient pollution (Brodie on a variety of substrata, with several reports et al. 2007) and the species may have been of occurrence on stones (Kann 1993, Kusel- regionally extirpated (Wehr 2011). Similarly, Fetzmann 1996, Kahlert et al. 2002), as an epi- Friedrich et al. (1984) documented that all 4 phyte on higher plants or other algae (Kirkby species of freshwater brown algae known from et al. 1972, Szymanska and Zakrys 1990, Young Germany are listed as endangered to different et al. 2010), and even as an endophyte in a few degrees. This includes the population of Pleu- instances (Waern 1952). Kann and Tschamler rocladia lacustris from its type location in Ger- (1976) demonstrated that the alga also colo- many, where it was first described by Braun in nizes artificial substrata (plastic and glass 1855 and where it is now listed as threatened slides) in suitable habitats. Given these eco- with local extinction (Geissler 1988). As of this logical limitations, this species may be geo- date, it is not known if this important popula- graphically limited by a restriction to calcare- tion still exists. ous habitats. The ecological data for P. lacustris assem- Pleurocladia lacustris was the first freshwa- bled so far indicate that the species is re - ter species of brown algae described; yet it is stricted to fairly nutrient-rich, alkaline, cal- an enigma with regard to its ecological re - careous environments (Israelsson 1938, Waern quirements and geographic distribution. With 1952, Kusel-Fetzmann 1996) and that it is freshwater and brackish water populations, absent from softwater or humic-stained sys- and relatively few known locations, the dis- tems (Kann 1940, Eloranta et al. 2011). A sin- covery of new populations is noteworthy. gle sample in June 2010 taken from one of our Further biodiversity surveys may clarify the sites (Salmon Creek) by the Surface Water extent to which P. lacustris may be a rare Ambient Monitoring Program of the California species. But, given its widespread locations State Water Resources Control Board indi- separated by long distances, 4 broad questions cated moderately high specific conductance emerge: (1) Is “Pleurocladia lacustris,” as re- (372 mS ⋅ cm–1), very low TDP (9.5 mg ⋅ L–1), ported, one species or several? It may be that TDN 63.6 mg ⋅ L–1, and alkaline pH (8.5) but while its morphological characteristics are clearly nonsaline. These data collectively indi- highly consistent among populations, isola - cate that the alga occurs in systems with pH tion and divergence may have resulted in sev- >7.5 and specific conductivity >200 mS ⋅ eral cryptic species, as demonstrated in other cm–1. No extensive analyses of water chem- freshwater and marine taxa (Casamatta et al. istry requirements exist yet for this species. 2003, Saunders 2008). Future genetic analyses However, preliminary lab experiments suggest will shed light on this question. (2) If its distri- that P. lacustris may tolerate a wide range of bution is restricted, is P. lacustris limited by its phosphorus conditions through the production ecological requirements or perhaps by disper- of hyaline hairs (Wehr 2003). Hyaline hairs in sal? Field data suggest that this species pre - other species have been documented to utilize fers calcareous conditions, but detailed experi- organic-P sources (Gibson and Whitton 1987). ments are needed to confirm either factor as a Pleurocladia lacus tris has been collected from cause of its ecological and geographic restric- small ponds to very large lakes (e.g., Klebahn tion (e.g., Telford et al. 2006, Boedeker et al. 1895, Kirkby et al. 1972, Kahlert et al. 2002, 2010). (3) Is P. lacustris a rare species or eco- Young et al. 2010), as well as from streams and logically restricted? Though habitat destruc- rivers (Eken stam et al. 1996, Kusel-Fetzmann tion has reduced its distribution in some areas, 1996, this study). P. lacustris could still be undersampled or Interestingly, in addition to occurring in a missed in biodiversity surveys. New surveys number of fully freshwater systems, P. l a c u s - can employ molecular methods, such as ge- tris has been reported from brackish environ- nome shotgun sequencing and DNA bar- ments, often in areas where limestone is pres- coding, to reveal hidden biological diversity ent (Waern 1952, Wilce 1966, Konan-Brou and and the presence of underreported taxa (e.g., 154 WESTERN NORTH AMERICAN NATURALIST [Volume 73

Eisen 2007). (4) What is the relationship be - DITTAMI, S.M., A. GRAVOT, S. GOULITQUER, S. ROUSVOAL, tween freshwater and brackish (intermittently A.F. PETERS, A. BOUCHEREAU, C. BOYEN, AND T. TONON. 2012. Towards deciphering dynamic changes marine) populations of P. lacustris, both in and evolutionary mechanisms involved in the adap- terms of ecological adaptations and evolution? tation to low salinities in Ectocarpus (brown algae). Laboratory studies can elucidate the ability of The Plant Journal 71:366–377. near-coastal and inland populations to adapt to EISEN, J.A. 2007. Environmental genome shotgun sequenc - a range of salinities (e.g., Dittami et al. 2012), ing: its potential and challenges for studying the hid- whereas population genetics studies may ex - den world of microbes. PLoS Biology 82:384–388. EKENSTAM, D., E.G. BOZNIAK, AND M.R. SOMMERFELD. plain the evolutionary route this species may 1996. 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Prodromus einer Roten Liste der Cyanobakterien/Blaualgen, Rot-, Gelbgrün-, Braun- 156 WESTERN NORTH AMERICAN NATURALIST [Volume 73 EMarine19 EBrackish14 EEBrackish15 EMarine12 EEMarine12 EMarine12 BrackishEBrackish22 EMarine26 E FreshwaterEE 21, 22 E 23 Freshwater Freshwater Freshwater Freshwater 29 7, 10 6 6 EMarine30 EMarine18 EMarine30 EEMarine24 EEEBrackish15 EBrackish29 FreshwaterEE FreshwaterE FreshwaterE 29 EBrackish20 Freshwater 6 Brackish 6 Freshwater Freshwater 3 29 8, 13, 31 2 EMarine19 EEEEEBrackish9 E 25 Freshwater Freshwater Freshwater Freshwater Brackish 16 16 16 17, 27 EEE Freshwater Freshwater Freshwater 6 6 6 EMarine18 ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° cal order at the end of appendix; * = present study. 4.023402 5.657824 6.915093 18.766667 69.272016 56.131528 51.726107 84.433265 53.657538 – – – – – – – – – N NNNNNN 24.947785 N 20.331188 N 15.442536 N 23.112942 N 53.698906 N 59.197774 N 50.255892 17.095460 18.575646 18.696536 18.664866 N N NN NNNN 12.414937 NN 11.564225 N 12.414522 N 26.233190 N 7.123362 N 13.258528 9.739689 10.410463 8.278405 11.826076 N NNNNNN 16.555300 16.498241 16.344250 13.542835 4.805384 NN 18.544724 18.654903 N 140.936332 N N 18.615049 ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° ° 38.046684 − worldwide. Many early reports lack precise latitude and longitude unless specific place names were provided Pleurocladia lacustris . Listing of all known populations PPENDIX A Ivory CoastLatviaLatviaNorwayPolandRussiaRussiaRussia / Kazakhstan AbidjanSpainSwedenSweden Baltic SeaSweden Eastern Gotland Basin, Baltic Sea Sweden N. Caspian Isfjoden 78.229253 SeaSweden Lake Wigry Zemlya Novaya Island Vaygach Gijón Lake Malaren Lake Erken Stream in Lundakvarn Stream in Söderby-Karl, Risslingby 56.833476 Stream in Rönsbol 5.265194 45.534226 56.797271 59.855306 70.818962 54.030562 69.916202 59.758277 59.514982 59.845040 59.825018 43.535064 Greenland Havnenaes (E. Greenland) Vestre Supralittoral, 76.750000 Greenland Greenland) Qaanaaq (W. Supralittoral, 77.582952 DenmarkDenmarkDenmarkDenmarkFinland/ Estonia FranceGermanyGermanyGermany Lake FuresøGermany Islands Supralittoral, Faroe Baltic Sea Gulf of Finland, Germany / Poland Sjaelland Ditch, Tystrup, Greenland Lake Furesø Stream of the Brague, Antibes Berlin See, N. Tegeler Eastern Lakes around Baltic SeaBaltic Sea Lake District Plön Upper Rhine River Greenland) Upernavik (W. Supralittoral, 61.982669 59.860721 55.362147 43.609023 55.794084 72.787298 52.579755 54.499488 55.784222 54.394801 54.149453 48.989997 Greenland Greenland) Nuuk (W. Supralittoral, 64.179959 (negative latitude = southern hemisphere; negative longitude values west of the prime meridian). Sources are listed in numeri AustriaAustriaAustriaAustriaBelgiumCanada (stream) Wasenbruck (stream) Fischa-Dagnitz Haschendorf (stream) Traunsee Lake region Antwerp Supralittoral, Devon Island 48.025307 47.986840 47.886570 75.699993 47.861839 51.360796 SwedenSweden Norrjarsjo, inflow stream to Lake Erken Stream in Estuna, Norrmalma, Lake Erken 59.837317 59.854766 CountryAustralia Site location description MacDonnell Port Ponds, Piccaninnie Greenland Latitude Greenland) Holsteinborg (W. Supralittoral, Longitude 66.928933 Habitat Source 2013] FRESHWATER PLEUROCLADIA IN CALIFORNIA 157 . [2010]. Alkaline . Relationships of A. Br. Und deren A. Br. . 1982. El herbario de ANSCH . 1966. Novye I interesnye -epiphyte assemblages: regu - -epiphyte assemblages: regu IRERA UNNARSSON L.A. P -C in Arctic North America. Journal . 1990. New phycological records K. G AND EREZ , Cladophora AND AKRYS ABERZINSKAJA , Pleurocladia lacustris J.L. P UCKER B. Z Pleurocladia E.B. Z E.B. AND IELSEN AND AND , S., , S., , N.N. 1932. K poznaniu flory I rastitelnosti vodor- , N.N. , L.I.J. 1938. Materiaux pour servir a la Flore algo- , H., EEE Freshwater Freshwater Freshwater 11 4 32 EEEE Freshwater Freshwater Freshwater Freshwater 5 * * * EEBrackish29 EBrackish15 EBrackish15 EBrackish15 EBrackish1 FreshwaterE 6 Freshwater 28 , I., R. N ° ° ° ° ° ° ° ° ° ° ° ° ° ° EEL , M. 1952. Rocky-shore algae in the Öregrund Archipel- , A.D., , A.D., , N. 1895. Über , E.B., R.C. T , E.B., , R.T. 1966. M ILLE ILCE AERN ORONICHIN ITTLEY ALENZUELA AN INOVA OUNG ZYMANSKA algal floras in North Atlantic Islands (Iceland, the Faroes, the Islands (Iceland, the Faroes, algal floras in North Atlantic Proceedings 2005:33–52. Shetlands, the Orkneys). BIOFAR sytematische Stelling. Berichte der Deutschen Botanischen Gesell - Berichte der Deutschen Botanischen Gesell sytematische Stelling. schaft 13:106–112. osles presnych vodoemov Kryma. Botanicheskie. Zhurnal SSSR 17:265–325. phosphatase in freshwater logique de la Province d’Anvers. Premier Supplement. Bulletin de la Société Royale Botanique Belgique 71:34–40. lation in response to phosphorus supply and localization. Journal of Phycology 46(1):93–101. from Poland. Algological Studies 60:25–32. from Poland. vodorosli Kaspijskogo Morja. Algae novae ac curiosae Maris Cas - vodorosli Kaspijskogo Morja. Algae novae ac curiosae Maris Cas Rastenil 1966:109–114. pici. Novosti Sistematiki Vysshikh ago. Acta Phytogeographica Suecica 30:1–298. ago. Acta algas marinas Espanolas de F. Miranda. Collectanea Botanica 13: algas marinas Espanolas de F. 945–975. of Phycology 2:57–66. W T V V Y V W S Unpublished website: http://data.gbif.org/occurrences/98432509 W Z 23 24 25 26 27 28 29 30 31 32 33 1.547046 86.078867 87.873910 – 109.421503 121.358070 121.407284 121.458961 – – – – – – N N N N N N NNNNNN 17.612617 N 18.515715 N 20.522091 19.253617 19.880109 29.113328 34.112949 ° ° ° ° ° ° ° ° ° ° ° ° ° ° . 2009. Species and Pleurocladia lacustris . 1925. Die Sußwasser- IGULA 1994. Available algal biomass 1994. Available CHUBERT W. M H. S , editors. 2012. HELCOM 2012 UIRAL AND AND , D. G ALDIN , J. H AND ELIG in Lettland. Hedwigia 65:331–340. CHILLER , E.L. 1996. New records of freshwater Phaeo- AND , L.K. Meddelelser om 1893. Grønlands havalger. , A.A., , L.K. 1910. On the marine algae from north-east , F.R. 1877. Om Spetsbergens marina, klorofyllforande , F.R. , D., U. S U. , D., , T., , T., , H. 1895. Beobachtungen über ROU ETZMAN , A., J. S , A., J. -B -F Lithoderma , H. 1925. Bemerkungen über die Süßwasserarten der Gat- zu einer Algenflora von Lettland IV. , H. 1928. Vorarbeiten ONTULA LEBAHN OSENVINGE JELLMAN USEL OSENVINGE ONAN CHORIES ASCHER KUJA KUJA A. Br. Berichte der Deutschen Botanischen Gesellschaft 13: A. Br. 93–106. Grønland 3:763–981, 57 figs. + 2 plates. synonym list of the German marine macroalgae based on histori- cal and recent records. Rostocker Meeresbiologische Beiträge 21: 7–135. Greenland (N. of 76 N. Lat.) collected by the “Danmarks Expedi- of 76 N. Greenland (N. tion.” Meddelelser om Grønland 43:122–123. phyceae from lower Austria. Nova Hedwigia 62:79–89. phyceae from lower Austria. tung Horti Botanici Universitatis Latviensis 3:103–218. Acta Checklist of Baltic Sea macro-species. Baltic Sea Environment ings No. 130, Helsinki Commission, Helsinki, Finland. Proceed Flora Deutschlands, Österreichs und der Schweiz. Heft 11, Hetero - Flora Deutschlands, Österreichs und der Schweiz. Heft 11, Hetero Jena. Fischer, kontae, Phaeophyta, Rhodophyta, Charophyta. G. Thallophyter. II. Bihang till Kongl. Svenska Vetenskaps–Akade - Svenska Vetenskaps–Akade II. Bihang till Kongl. Thallophyter. miens Handlingar 4:51–52. in tropical brackish water artificial habitats. Aquaculture 119: in tropical brackish water artificial habitats. Aquaculture 175–190. R K K R S K K K P S S 12 13 14 15 16 17 18 19 20 21 22 . , in the . 1996. ETTERSON 144. – Pleurocladia . 2008. A sur- K. P . 1972. AND OMMERFELD KUDAN , HITTON E.S. O E.S. M.R. S Pleurocladia lacustris ILLEBRAND AND , AND B.A. W , . 2001. Distribution and abundance of , H. H URAL AND , (Phaeophyta) in North America. Journal OWE OZNIAK , B. D , B. IBBERD ASSELROT R.L. L 114, 6 plates. Leipzig, Germany. 114, 6 plates. Leipzig, − RDUGAN AND 1. Continued. Pleurocladia , G. 1938. Über die Süßwasserphaeophyceen Schwe- A. Braun (Phaeophyta)—a new British record. Vasculum , D., E.G. B E.G. , D., , D. 2006. Litorale Aufwuchsalgen im Hoch- und Ober- , D. 2006. Litorale Aufwuchsalgen , M., A.T. H A.T. , M., , S.M., D.J. H D.J. , S.M., , R.L., , E. 1993. Der litorale Algenaufwuchs in See Erken und , A. 1855. Algarum unicellularium genera nova et minus cog- , V., H. E , V., , E. 1978. Systematik und Ökologie der Algen Österreich - , E. 1978. Systematik und Ökologie der Algen Österreich , E. 1940. Ökologische Untersuchungen an Litoralalgen osthol - , E. 1940. Ökologische Untersuchungen an Litoralalgen osthol PPENDIX ANN IRKBY littoral zone of northeastern Lake Michigan [abstract]. Proceed- La Crosse, WI. ings of the North American Benthological Society, ischer Bergbiiche. Arch. Hydrobiol. Suppl. 53:405–643. rhein. Carolinea 64:5–68. seinem Abfluß (Uppland, Schweden). Algological Studies 69:91–112. A Journal vey of marine algae and seagrasses Istanbul, (Turkey). 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Freshwater Freshwater KENSTAM ARTER ANN AHLERT ANN ACKHAUS RAUN YSEL K SRAELSSON K E K I A B B C K K United StatesUnited StatesUnited States NE Lake Michigan, Sleeping Bear Dunes, MI W Lake Michigan, near Milwaukee, WI Flaming Gorge, UT Green River, 44.910114 43.060744 40.912815 United StatesUnited StatesUnited States Salmon Creek, CA Creek, CA Villa Creek, CA Willow 35.815765 35.849451 35.894091 CountrySwedenSwedenEstonia/ Sweden Sweden / FinlandFinland/ Sweden TurkeyUkraineUnited Kingdom Site location description Baltic Sea proper Northern Aland Sea, Baltic Kleringe Stream in Vendel, Sea & The Quark, Baltic Bothnian Öregrund Archipelago Durham Ponds, Brasside Infralittoral Bosphorus, near Istanbul1 Crimea Rivers, 2 3 62.793997 58.694637 60.149929 4 Latitude 41.175102 60.356942 5 60.100433 54.802017 6 Longitude7 44.946588 8 Habitat9 10 11 Source