RHODORA, Vol. 103, No. 914, 72-201. 2001 pp. 1 FROM A MUSCOIDES-LIKE FUCUS A MAINE SALT AND MARSH: ECOLOGY, ORIGIN, ITS TAXONOMIC IMPLICATIONS Arthur and Clinton Dawes C. Mathii;son' 2 J. Department of Planl Biology and Jackson Kstuarine Laboratory, New NH University Hampshire. Durham, 03824 oi' 'e-mail: arthurO^ hopper.unh.edu; 2e-mail:cdawes@chumal .cas.usr.edu abstract. The morphology and habitat dwarf moss-like or nuiscoi- o\' a des-like fucoid brown alua were studied in the Brave Boat Harbor sail marsh of York-Kittery, Maine, U.S.A. using transect studies and transplant experi- ments. The plant, which lacks a holdfast, forms a dense embedded turf amongst sparse Spartina patois populations the high marsh, particularly in on well-drained sandy sediments near the Harbor's mouth. The plant's di- chotomously branched were fronds smaller than those previously reported for mm mm = muscoides-like populations from Europe (mean 13.2 long, 1.1 wide, and 0.1 g damp-dried weight), while they had a similar dominance oi marginal hair pits or cryptostomata. Transplantation in situ Fucus spiralis o\' from the lower to the upper marsh resulted in enhanced fragmentation, stunt- ing, proliferation, and reduced reproduction. Reciprocal transplantation of the muscoides-like Fucus from upper lower elevations caused enhanced frond to length and proliferation. Based upon detailed transplant and morphological we studies, conclude that the muscoides-like Fucus plants from Brave Boat Harbor represent a phenotypic variant of F. spiralis, caused by detachment, extensive proliferation, and subsequent degeneration detached fragments. oi' The plant's dwarf morphology primarily linked to a series unique en- is o\' vironmental conditions (desiccation and low nutrients), plus the type o\' at- tached parental material available. Thus, the dwarf muscoides-like Fucus in some may luii'ope and Northwest Atlantic sites be derived from F. vesieu- An while Brave Boat Harbor losus, in the parental material F. spiralis. is analogous pattern also evident between Ascophyllum nodosum and de- is its tached ecad scorpioides, with the presence of dwarf specimens and the oc- currence of conspicuous morphological continuum between two a the plants. Key Words: Brave Boat Harbor Maine, ecad ecologv. fucoid alizae. salt marsh seaweed development, taxonomy algae, common Seaweeds that lack holdfasts (free-living) are through- embay men out the world, particularly within protected salt ts, marshes, and estuaries (Norton and Mathieson 1983). The tem- perate North Atlantic fucoid genera Ascophyllum and Fucus con- tain several free-living marsh plants (Baker and Bohling salt which 1916; Fritsch 1945; Niell 1980), can contribute major et al. quantities of biomass and primary productivity (Brinkhuis 1976; 172 — Dawes Mathieson and Muscoides-like Fucus 173 2001] Chock Ma- Brinkhuis and Jones 1976; Brinkhuis 1976; and et al. thieson 1976). Several positive interactions occur between salt marsh flowering plants and unattached fucoids, including reduced desiccation and enhanced survival of A. nodosum (L.) Le Jolis (Hornemann) ecad scorpioides Reinke, plus increased cordgrass biomass due enhanced sediment (Spartina alterniflora Loisel.) to (Chapman Chapman The nutrients and 1999; Gerard 1999). tax- onomy of unattached fucoids poorly understood (Fritsch 1945; is Norton and Mathieson 1983; Sears 1998), with plants being var- megaecads, and (Bak- iously classified as ecads, species, varieties Wynne Mag- and Bohling 1916; Sears 1998; Taylor 1957; and er The morphology ne 1991). "altered" of free-living fucoids, which includes dwarfing, spiral twisting, profuse branching, veg- etative propagation, and the lack of a holdfast (Baker and Bohling Norton and Mathieson 1916; Fritsch 1945; Niell 1980; et al. The 1983) has contributed these taxonomic problems. varied to morphologies of free-living fucoids have been attributed to re- duced nutrients and/or sluggish currents, and enhanced salinities, Chapman desiccation (Boney 1966; 1964). In discussing the or- emphasizes igin of free-living fucoids Fritsch (1945) that they "are derived by vegetative propagation from saxicolous all types/' One embedded of the most unique marsh fucoids the dwarf, is moss-like Fucus frequently found within upper marsh- that salt is 5-6 es of Europe and the British Isles. It is described as being mm cm having compressed branches (1-3 cylindrical to tall, wide), and bearing marginal hair or cryptostomata Fritsch pits (cf. Lynn Newton and Cooke 1945; Jorde 1966; 1935; 1931; Valera Although anchored 1979). lacking a holdfast, the plant is (i.e., partially embedded) in firm sand or peat-like sediments within Magne high marshes (Cotton 1912; Feldmann and 1964; tidal Lynn Norton and Mathieson Muscoides-like Fucus 1935; 1983). plants have been variously designated as varieties (Cotton 1912; Lynn 1935), ecads (Baker and Bohling 1916; Niell et 1980), al. Magne (Feldmann and Parke and or as distinct species 1964; Wynne Magne Dixon 1976; and 1991). In Cottoirs (1912) initial characterization of muscoides-like Fucus, he treated taxo- this it nomically as F. vesiculosus L. muscoides and described as var. it forming moss-like carpets swards) within the high intertidal (i.e., zone Clare Subsequently Baker and Bohling Island, Ireland. at (1916) designated the plant as F. vesiculosus ecad muscoides, Rhodora 174 |Voi. 103 emphasizing that was part of a morphological cline within the it megaecad limicola Baker Bohling (Clements 1905); the ecads et caespitosus Baker Bohling, Agardh, nanus et filiformis J. J. Agardh, subecostatus Agardh. and (Hudson) Turner volubilis J. were megaecad also included within the limicola of F. vesiculo- Feklmann Magne and sus. (1964) elevated F. vesiculosus var. On muscoides to a distinct species, F. muscoides. the other hand, during recent survey of Spanish vesiculosus populations, a F. Niell (1980) agreed with Baker and Bohling's (1916) et al. inter- pretation, designating various ecads within vesiculosus megae- F. cad limicola and showing gradation of morphology ranging a from F. vesiculosus axillaris to F. vesiculosus ecads volubilis, f. caespitosus, and muscoides. Wynne Magne and (1991) also agreed with Feklmann and Magne (1964), stating that this plant should be recognized the at name However, employed species level. they pointed out that the Magne by Feklmann namely Fucus muscoides (1964), (Cotton) et Feldman and Magne, homonym now created a later of a red alga known Acanthophora muscoides Bory as (L.) de Saint- Vincent new (1828). Accordingly they proposed a name, F. cottonii M. Wynne Magne, honor of A. D. Cotton, suggesting et in that J. the dwarf morphology and unique ecological niche within high marshes tidal clearly delineated the taxon. The was present study undertaken after a investigation floristic of seaweeds within Brave Boat Harbor, York-Kittery, Maine, U.S.A. (Figure revealed the occurrence of a muscoides- 1) first Fucus North America (Mathieson like plant in et 2001). In the al. we summarize present account detailed morphological, ecologi- and cal, transplant data regarding these unique populations, in order taxonomy, and to clarify the plant's origin, biology. MATERIALS AND MITMODS Mathieson et al. (2001) have given a detailed characterization of the Brave Boat Harbor marsh (43°06.0'N, 70°39.33'W; salt BBH), hereafter including geography, hydrographic conditions its (temperature and composi- salinity), habitat variability, species tion, and site locations within the main tidal channel and four The contiguous biomass mus- tidal tributaries. patterns for the Fucus and marsh were coides-like other plants recorded salt at seven transect sites along the main tidal channel (Fimire with 1), — Dawes Mathieson and Muscoides-like Fucus 175 2001 MAINE BRAVE BOAT HARBOR 43°05' OCEAN ATLANTIC 70°44' 70°43'40" Figure Brave Boat Harbor. York-Kiltery. Maine showing the location I. of seven transect sites within the main tidal channel. See Figure in I Maine Mathieson (2001) for details of the southern coast. et al. mean Table Distribution and biomass of dominant seaweeds and flowering plants on seven transects within Brave Boat 1. % Harbor. Maine. Symbols: = percent occurrence, X = present, and mean biomass = g dry wt./m 2 ± SD (± SE). 1 1 # Mean Site 2 4 6 Biomass 3 5 7 1 Distance inland from mouth (km) 0.29 0.31 0.38 0.40 0.79 0.86 1.12 present) (sites 9c f SEAWEEDS Ascophyllam nodosum Le X (L.) Jolis 28.6 20.5 14.8 (10.6) Ascophyllum nodosum Le (L.) Jolis ecad scorpioides (Hornemann) Reinke X X X X X X 85.7 868.2 1255.0 (500) 70 Fucus "muscoides-like" x X X X X X X sp. 100 266.3 122.3 (46.2) o Fucus X X X X X X spiralis L. 85.7 327.8 395.0 (161.4) o Fucus spiralis L. X ecad Sauvageau lutarius (Kiitzing) 14.3 130.0 94.8 (94.8) Fucus vesiculosus L. ecad (Hudson) Turner X X volubilis 28.6 647.8 590.8 (341.5) Melanosiphon X X X X intestinalis (D. A. Saunders) 57.1 378.6 124.0 (62.0) Wynne M. X X X X X X X J. 100 12.6 108.8 (41.1) 1 Rhizoclonium riparium (Roth) Harvey X X X X X X X 100 112.6 108.8 (41.1) Vaucheria spp. TOTAL SEAWEEDS/SITE 6 7 6 6 6 6 5 < c oj to o Table Continued, 1. Ef Site # ? 3 4 5 6 7 Mean Biomass 1 o Distance inland from mouth (km) 0.29 0.31 0.38 0.40 0.79 0.86 1.12 (sites present) 9? 'O % [Mean # taxa 6.0 0.57; Mean 66.9 35.1%; Mean Biomass present) = 313.8 ± 281.0 dry wt./m 2 (sites (93.7) g ] FLOWERING PLANTS X ± Festuca rubra L. 28.6 5095.7 4159.2 (2949.8) c Limonium x X X X ± Small nashii 85.7 226.0 229.6 (93.7) C/3 X europaea Salicornia L. 14.3 28.0 38.9 (38.9) X X X X X Spartina alteruiflora Loisel. 85.7 298.6 367.0 (149.8) Spartina patens (Aiton) Muhl. X X X X 100 915.9 968.9 (365.6) O Suae da Dumort. X maritime* (L.) 14.3 253.0 238.3 (238.3) o x Triglochin maritima L. 14.3 63.0 89.1 (89.1) CD TOTAL FLOWERING PLANTS/SITE 2 3 4 3 5 5 2 i % [Mean # taxa = 3.4 ± 1.3; Mean 49.0 39.4%; Mean Biomass (sites present) = 982.8 ± 1836.9 (693.2) g dry wt./m 2 ] Rhodora 178 Vol. 103 I km km these sites varying from 0.29 to 1.12 inland from the mouth. Elevation records were determined using a line level and (Dawes a surveying rod 1998; Mathieson 1998). with ver- et al. MLW) mean heights above or below low water being tical (i.e., from (Harbor Master Program. calculated predicted tidal levels The Version Zihua Software, Marlboro. CT). delay 3, in tidal rise inner transect was calculated by subdividing the main for sites channel into four 15-minute increments that matched the one- hour delay noted the innermost part the marsh. at o\^ May were conducted between and Transect studies (Figure 1) September, 1998 seven Metered of variable lengths at sites. lines (5-7 m), depending upon shore topographies, were established al right angles to the shoreline, extending from the tidal channel to the high marsh community dominated by SparUna patens (Ailon) A minimum Muhl. two biomass cores per meter were taken oi^ cm along each transect with a polyvinylchloride tube (95 2 par- ), when ticularly conspicuous vegetational changes occurred or where the muscoides-like Fucus was evident. Each core was la- beled and returned to the laboratory within one hour where was it stored 10°C being processed. Ultimately the macroalgae until at and marsh plants within each core were separated and their salt damp-dried biomass values converted dry wl./m 2 using wet to g a A com- dry weight conversion determined each to for species. mean parison species composition and biomass for the seven o\' transects summarized (Table Morphological assessments o( is ). 1 live the six fucoid taxa found were made, including Fucus oi' nodosum spiralis L., Ascophyllum (L.) Le Jolis ecad scorpioides (Hornemann) Reinke, spiralis ecad lularius (Kutzing) Sauva- F. geau, F. vesiculosus L. ecad volubilis (Hudson) Turner, and the Fucus muscoides-like (Figures 2 and 3). cm Fucus Reciprocal transplants of cores (92 2 containing spir- ) and muscoides-like Fucus were during June alis plants initiated km 1998 at a site located 0.38 inland from the mouth along the BBH. made main channel were from tidal Vertical transfers oi' MLW m + 2.0 to +3.4 above and vice versa, with four different types oi populations being assessed: high populations situ (1) in muscoides-like Fucus mixture fragmented or a spiralis F. oi' oi' ecad and muscoides-like low lutarius plants; (2) in situ F. spir- low were from transplants or plants transferred the alis: that (3) higher to the lower fucoid /one; and (4) high transplants or plants that were transferred from the lower to the higher fucoid zone. — Dawes Mathieson and Muscoides-like Fucus 179 200 i | cm 2 D V E V A. J < v ( m ^ u v 1) v- vh > f ^ 5 • 1 G H F Figure Silhouettes of morphological variability three fucoid popu- 2. in lations from Brave Boat Harbor. Attached Fucus spiralis ranging from germl- ings (A. group ol' 8). to a pair of reproductively mature adults (B), to residual and proliferous specimens (C, group o( Detached specimens of F. spiralis 5). more ecad lutarius grading from large, fragmented fronds (D, group of to 5), proliferous, smaller plants (E, group Turf-like populations of muscoi- o\' 8). des-like Fucus ranging from tufted, elongated specimens (F, group o\' 12). to short, individual fronds (G, group of 18), to minute plants (H, group of 22). Rhodora 180 Vol. 103 | A B C >£7 y r D cm H 2 Figure Silhouettes of morphological variability two fucoid taxa from 3. in Brave Boat Harbor, Maine. Detached Ascophyllum nodosum grading from two more large fragments (A), to a pair of proliferous fragments (B). to progres- sively smaller fronds (C, group of and finally to minute plants of the ecad 6), scorpioides (D, group of Attached (E) and detached fronds of Fucus II). vesiculosus (F) grading into F. vesiculosus ecad volubilis (G, group of 3), and then more proliferous and smaller residual specimens (H, group of to 3). — Dawes Mathieson and Muscoides-like Fucus 2001] 181 Tabic Sediment characteristics of core samples (top 5 cm) from each 2. of seven transect sites within Brave Boat Harbor's main tidal channel. The SD ± means data represent percentages of total values based on the of 1 duplicate cores. % SD Mean ± 12 composition total 1 Site # 3 4 5 6 7 Distance inland (km) 0.29 0.31 0.38 0.40 0.79 0.86 1.12 Water content (%) 26.0 30.0 37.0 36.0 51.0 54.0 55.0 ±0.9 ±2.4 ±1.2 ±1.5 ±2.3 ±0.5 ±0.7 Medium 70.0 55.0 58.0 58.0 30.0 32.0 33.0 size particles mm) (> 0.125 ±8.1 ±6.6 ±8.8 ±14.0 ±7.4 ±7.4 ±3.1 Fine sand, parti- 3.0 3.0 4.0 5.0 10.0 11.0 11.0 silt mm) (< 0.063 ±1.0 ±1.3 ±1.3 ±1.3 ±1.7 ±2.5 ±3.4 cles Thus, the terms low and high transplants refer to the resulting rather than the materials. Duplicate cores of each situ initial in were biomass and population taken order evaluate in to initial morphometric patterns (see below). The transplant samples were harvested approximately one year June 1999) and sev- after (i.e., morphometric were compared with previous eral features in situ materials (see above). Replicate core samples individual transect were pooled at sites and the frond morphology of 25 plants assessed, including their (mm) length (cm), width (mm), weight burial depth or the (g), numbers blackened zone due anoxic conditions, of branches to and and numbers of marginal and cryptos- fertile tips, surficial Only tomata or hair pits (cf. Niell el al. 1980). flattened fronds of Fucus plants were assessed for cryptostomatal patterns, as the small cylindrical branches of the muscoides-like Fucus had few compared cryptostomata and could not be directly with other flat- tened taxa. Cryptostomatal ratios were assessed using a represen- mean and ocular (100 X). Ultimately, values standard tative field deviations for each of the above described morphometric param- were eters calculated. Sediment and water content were determined particle size at each of the seven transect sites (Table using a stainless steel 2), cm cm were tube (11.3 2 Duplicate cores (10 long) extracted at ). each within dense populations of muscoides-like Fucus and site placed in individually labeled plastic bags that were returned to the laboratory. Samples were either processed immediately or re- The above-ground ma- 10°C frigerated for later analysis. plant at