WETLANDS, Vol. 29, No. 1, March 2009, pp. 163–175 ’ 2009, The Society of Wetland Scientists
TAXONOMIC COMPOSITION AND DIVERSITY OF MICROPHYTOBENTHOS IN SOUTHERN CALIFORNIA MARINE WETLAND HABITATS Christopher N. Janousek Scripps Institution of Oceanography, University of California, San Diego, La Jolla, California, USA 92093-0218 Current address: Department of Plant Pathology, University of California, Davis, California, USA 95616. E-mail:
[email protected] Abstract: Sediments in coastal wetlands host communities of phylogenetically diverse primary producers such as diatoms, cyanobacteria, and anoxygenic photosynthetic bacteria, but little is understood about spatial variation in the composition of these assemblages at the highest taxonomic levels. Using High Performance Liquid Chromatography to quantify taxon-specific pigments, I investigated habitat-linked heterogeneity in microphytobenthic biomass, composition, and diversity within two natural wetland systems from southern California and tested for differences in community structure between natural and restored ecosystems. Natural vegetated habitat at Mission Bay had higher concentrations of zeaxanthin (cyanobacteria) and bacteriochlorophyll a (anoxygenic photobacteria) than unvegetated mudflat and creek banks. Organic matter was positively correlated with the concentrations of these pigments, whereas sediment pore water salinity and sand content were generally unrelated to composition. At Tijuana Estuary, community structure was generally similar between mudflat and Spartina marsh at the natural site, but concentrations of chlorophyll a and fucoxanthin (diatoms) were higher in mudflats. Restored wetland similarity with adjacent natural habitat (age 2 yr at Tijuana Estuary and 6 yr at Mission Bay) depended on habitat type and pigment measure. Restored upper intertidal succulent marsh at Mission Bay was most divergent: it had lower microalgal biomass, a lower concentration of zeaxanthin relative to fucoxanthin, and less bacteriochlorophyll a relative to chlorophyll a than natural habitat. The results suggest that patches of prokaryotic primary producers coincide with areas of high sediment organic matter and/or hypoxia superimposed on a broadly distributed flora of diatoms across various wetland landscapes. Key Words: anoxygenic phototrophic bacteria, bacteriochlorophyll a, cyanobacteria, diatoms, green algae, Kendall-Frost Mission Bay Marsh Reserve, mudflat, periphyton, Spartina foliosa, Tijuana Estuary, wetland restoration
INTRODUCTION
involve removal of higher elevation sediment next to existing wetlands, construction of intertidal channels, and/or the opening of estuary mouths that have closed due to sand deposition. In these tidal wetlands, benthic algae and photosynthetic bacteria form a functionally important component of salt marsh and mudflat communities (Miller et al. 1996). Microphytobenthic (or ‘‘microalgal’’) assemblages can include cyanobacteria, anoxygenic phototrophic bacteria, diatoms, and other eukaryotic algal groups (Pinckney et al. 1995, Sullivan and Currin 2000). Despite the tendency for many researchers to treat microphytobenthic assemblages as a single functional entity, communities of these phototrophs represent rich phylogenetic diversity with substantial variation in metabolic, physiological, and behavioral characteristics (Janousek 2005). This variability leads to the diverse ecological roles played by microphytobenthic assemblages in addition to primary production: nitrogen fixation
Extant wetlands along the coast of southern California are composed of various tidally influenced habitats of different sizes and histories. Mudflats, intertidal channels, high intertidal salt pans, and marshes hosting salt-tolerant grasses and succulents occur in spatial mosaics organized by hydrologic and geologic forces, natural disturbance, interactions between vascular plants, and coastal development (Redfield 1972, Callaway and Pennings 2000). Much of the coastal wetland habitat present in southern California during early historic times has been lost or heavily altered by human influence (Marcus 1989, Zedler et al. 2001). Wetland degradation has led to reduction of local biodiversity (Ibarra-Obando & Poumian-Tapia 1991, Zedler et al. 2001). To compensate for habitat loss, a number of wetland restoration projects have been implemented in the region (Zedler 1996) and typically 163
164 (Carpenter et al. 1978), sulfide oxidation (Stal 2000), nutrient flux regulation (Tyler et al. 2003), sediment stabilization (Austen et al. 1999), and trophic support of heterotrophs (Page 1997, Middleburg et al. 2000). The dynamics of ecosystem functions supported by algae and photosynthetic bacteria are dependent on spatial variation in abundance, composition, and diversity. The biomass (as measured by chlorophyll a) of sediment-dwelling algae and cyanobacteria may vary across a suite of scales in marine wetlands. Differences may correspond to gradients in elevation (Brotas et al. 1995), to specific wetland habitats (Sullivan and Moncreiff 1988, Pinckney and Zingmark 1993), or to changes in wave intensity and substrate (Plante et al. 1986). Chlorophyll a measurements, however, have distinct limitations: 1) they do not include the contribution that purple or green photobacteria make to total photosynthetic biomass, and 2) they cannot elucidate variation in the composition or diversity of assemblages that may be important to ecosystem function (Loreau et al. 2001, Zedler et al. 2001). Gradients coincident with tidal elevation influence microphytobenthic spatial heterogeneity. For example, cyanobacterial composition and diatom diversity differ with tidal height (Javor and Castenholz 1981, Underwood 1994, 1997). Using rRNA estimates of diversity, Rothrock and Garcia-Pichel (2002) noted lower diversity in assemblages of heterotrophic bacteria and cyanobacteria at higher intertidal elevations. However, other work at the species level suggests that benthic taxa are generally well distributed across the intertidal (only showing differences in abundance across zones), suggesting widespread dispersal and/or broad tolerance to a variety of environmental conditions (Stewart and Pugh 1963, Sage and Sullivan 1978, Zedler 1982, Saburova et al. 1995). Differences in microphytobenthic composition may also be driven by other environmental gradients or interactions with wetland organisms such as canopy-forming vascular plants. For example, the presence/absence and abundance of particular microphytobenthic species or taxonomic groups in wetland sediments may potentially be influenced by changes in sediment particle size, salinity, and degree of compaction (Underwood 1997, Zong and Horton 1998, Waterman et al. 1999), metazoan grazing (Hagerthey et al. 2002, Armitage and Fong 2004), and nutrient concentrations (Van Raalte et al. 1976, Pinckney et al. 1995). To date, studies of spatial differences in microphytobenthic composition and diversity in wetlands often limit consideration to only a single large taxonomic group such as the diatoms (e.g.,
WETLANDS, Volume 29, No. 1, 2009 Sullivan 1975, 1977, Sage and Sullivan 1978, Currin and Paerl 1998; but see Zedler 1982). Here I present pigment data on differences in microphytobenthic abundance, composition, and diversity across common wetland habitat types in southern California. I tested the null hypothesis that community structure (abundance, diversity and composition) was similar among mudflat, creekbanks, Spartina-dominated marsh, and succulentdominated salt marsh in natural wetland at Mission Bay, California and between mudflat and Spartina marsh at Tijuana Estuary. I then compared the community structure of these natural assemblages to samples from nearby restored habitats, estimating the magnitude of difference between natural and restored habitat. Lastly, using samples from Mission Bay, I quantified the strength of relationships between sediment characteristics (salinity, grain size, and organic matter) and the composition and diversity of benthic producers. METHODS Site Description The northeastern corner of Mission Bay (32u 479N, 117u139W) in San Diego Co., California contains remnant salt marsh habitat that was formerly part of a more extensive system covering much of the bay (Purer 1942, Levin 1982). A small restoration site was constructed adjacent to natural habitat and connected to the natural site via a single second order channel. Salt marsh in both restored and natural areas contains halophytes such as Salicornia bigelovii Torrey, S. virginica Linnaeus, Batis maritima Linnaeus, Jaumea carnosa Gray, Limonium californicum Heller, Suaeda esteroa Ferren and Whitmore, Frankenia salina (Molina) Johnston and Triglochin sp(p). Patches dominated by cordgrass (Spartina foliosa Trin.) are also present. Both restored and natural wetlands contain first and higher order intertidal creeks. Natural salt marsh is separated from sub-littoral habitat in Mission Bay by unvegetated mudflats. Tijuana Estuary is located just north of the U.S./ Mexico border in San Diego Co. (32u349N, 117u79W). It is one of the largest remaining wetlands in southern California but has also been reduced in size over the last 200 years (Zedler 1996). The estuary contains salt marsh dominated by S. foliosa or mixtures of other halophytes such as Salicornia spp. Small to moderate-sized channels and expanses of unvegetated mudflat separating creeks from salt marsh are also present. An 8 ha restoration site was created adjacent to natural salt marsh and opened to
Janousek, MICROPHYTOBENTHIC DIVERSITY IN MARINE WETLANDS tidal influence in February 2000 as part of a longer term attempt to increase aerial coverage of intertidal wetland (Zedler et al. 2001). The restoration site initially consisted of mudflat habitat and areas planted with S. foliosa and other species (Zedler et al. 2001). Field Sampling To assess habitat-level differences in microphytobenthic community structure, eight replicate locations were randomly sampled in Mission Bay from 26–29 March 2002 within each of the following habitats: unvegetated mudflat (MUD), unvegetated creek-banks (CRK), Spartina-dominated salt marsh (SPAR), and salt marsh with one or more other halophytic, often succulent, plant species, but low Spartina abundance (SUCC). All mudflat samples were collected within approximately 200 m of the edge of the marsh. MUD, CRK, SPAR, and SUCC habitats are generally situated along a gradient of increasing tidal elevation (Zedler 1977). Eight replicate samples were also collected from the same habitat type in adjacent restored wetland (except lower intertidal mudflat which was not present at this restored site). At each sampling location, cores of surface sediment were collected for analysis of photosynthetic pigments and sediment water content (0.85 cm diameter, 1 cm depth), sediment grain size and organic matter content (1.4 cm diameter, 1– 2 cm depth), and pore water salinity (1.4 cm diameter, several cm depth). At a subset of locations, light transmission through the plant canopy to the sediment surface was measured with a QSL-100 light meter (Biospherical Instruments Inc.) by dividing light levels near the sediment surface with incident irradiance approximately 1 m above the ground. From 7–8 April 2002, 48 sediment communities were sampled in natural and restored habitat at Tijuana Estuary as part of a longer-term study of wetland succession (Janousek et al. 2007). Twelve replicate samples were haphazardly collected from both MUD and SPAR habitats in both natural and restored sites (data for most pigments, especially bacteriochlorophyll a, are n , 12). Brownish sediments were usually targeted for sampling in Tijuana Estuary (areas with apparent macroalgal cover were excluded whereas smaller macroalgae, if present, were included in Mission Bay cores). Surface sediment for pigment analysis and determination of interstitial water content and salinity was collected similarly to that described for Mission Bay, except that pigment and water cores consisted of 2 subsamples taken to 0.5 cm depth (most living algal
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cells were probably in the upper few mm of the finergrained sediments). All sediments were frozen (280uC for pigments, 220uC for other analyses) following collection. At both sites, S. foliosa densities were obtained in SPAR habitat by counting living and non-living shoots exceeding about 10 cm height inside 0.25 m2 or 0.0625 m2 plots. Sediment pore water salinity was estimated in the field on a refractometer after pressing wet sediment through filter paper set inside a plastic syringe (estimates were used when salinity exceeded 100 psu). Sediment moisture content was obtained by measuring weight loss after drying at about 55–60uC. Sediments collected for organic matter and particle size (% sand) analyses were separated though a 63 mm sieve into large (sand + granules) and small (silt + clay) fractions. Each fraction was dried, weighed, and then treated with up to 30% hydrogen peroxide for up to a few months to oxidize organic matter (Carver 1971). Generally, after little evidence of further reaction, sediments were washed, dried, and reweighed. Organic matter was expressed as the combined weight loss of both fractions following H2O2 treatment divided by total sediment mass. The proportion of sand was calculated as the mass of inorganic particles exceeding 63 mm divided by the total mass of inorganic particles. Pigment Quantification The pigment content of sediments was quantified using High Performance Liquid Chromatography (e.g., Brotas and Plante-Cuny 2003). Based on determination of sediment water content, an appropriate volume of 100% acetone was added to samples to form a 90% acetone solution for pigment extraction. Pigments were extracted at approximately 0uC for about 24 hr and then filtered through cotton packed inside a Pasteur pipette (Goericke 2002). 250 ml water was added to 600 ml of sample extract and 100 ml of this mixture was injected into an AdsorbosphereH C18 HS, 3 mm stationary phase, reverse phase column (100 mm length, 4.6 mm diameter; Alltech Associates, Inc.) coupled to a C18HS guard column (5 mm stationary phase) and 0.5 mm in-line filter. The solvent gradients, derived from Brotas and Plante-Cuny (1996), adequately separated lutein and zeaxanthin (,0.3 min; see Janousek 2005). Carotenoid absorbance was measured at 450 nm on a Spectra 100 variable wavelength detector. Chlorophyll a concentrations were quantified with a Waters 470 fluorescence detector (excitation 5 430 nm, emission 5 674 nm). For determination of bacteriochlorophyll a concentra-
166 tions, an additional 100 ml sample aliquot was analyzed on a separate gradient modified from Goericke (2002). Separation occurred on an Adsorbosphere C18HS reverse-phase column (5 mm stationary phase particles, 150 mm length) coupled to a pre-column (5 mm stationary phase) and 0.5 mm pre-filter (Janousek 2005). Detection was by absorbance at 770 nm. Pigment elution times were compared with those obtained from monospecific algal standards (e.g., Thalassiosira, Dunaliella) and from purified bacteriochlorophyll a (Sigma-Aldrich, Inc.). Detector responses were converted to mg pigment per cm2 of surface sediment by accounting for calibration equations generated with pure pigment standards, the original volumes of 90% acetone used for extractions, and the surface area of sediment collected in the field. Chlorophyll a and bacteriochlorophyll a concentrations were used as estimates of oxygenic and anoxygenic phototroph biomass, respectively (Pinckney et al. 1995). The carotenoids fucoxanthin, lutein, and zeaxanthin were used to quantify the abundances of diatoms, green algae (+ plant detritus) and cyanobacteria (Pinckney et al. 1995, Jeffrey et al. 1997). The taxonomic composition and diversity of communities was characterized by three additional measures: A) bacteriochlorophyll a/chlorophyll a ratios for anoxygenic versus oxygenic phototroph biomass, B) zeaxanthin/fucoxanthin ratios for cyanobacteria versus diatom biomass (Pinckney et al. 1995), and C) Simpson’s diversity index (1/D 5 1/gpp2 where pp 5 group-specific pigment mass/total diagnostic pigment mass), a measure incorporating variation in both evenness and richness (Magurran 2004). Pigment concentrations in environmental samples can be affected by variation in irradiance (Falkowski and LaRoche 1991) and nutrient concentrations (Geider et al. 1988), in addition to reflecting differences in algal biomass. Thus, comparison of chlorophyll a or bacteriochlorophyll a concentrations between unvegetated and vegetated habitat (with inherently large differences in light) must be interpreted with caution. However, because fucoxanthin and zeaxanthin (Brotas and Plante-Cuny 2003), and chlorophyll a and bacteriochlorophyll a (Go¨bel 1978) respond similarly to changes in irradiance, using ratios of these pigments as measures of community composition should be less heavily influenced by habitat-level differences in light. In addition, restored versus natural comparisons of community composition made in this study (within a single habitat type) should be less affected by algal photoacclimation.
WETLANDS, Volume 29, No. 1, 2009 Statistical Analysis Habitat-level differences in environmental variables and pigment measures in natural wetland at both sites were tested with one-factor ANOVA and Fisher’s LSD post-hoc comparison of means (CoStat 6.101, Monterey, CA). Two-factor analyses (with habitat type and restoration status as main factors) were initially conducted (Janousek 2005), but these often resulted in significant interaction terms, complicating interpretation. Estimates of v2 (a statistic analogous to r2 in regression that measures the proportion of variability accounted for by one or more ANOVA factors) were determined following Hays (1994). Following habitat-level comparisons within natural sites, pigment data from restored wetland assemblages were compared to natural habitat with one-way ANOVA for each habitat type at both sites. For each restored versus natural comparison, the magnitude of observed difference was quantified with Hedges’ Response Ratio where L 5 ln(meanrestored/meannatural) and 95% confidence intervals 5 L 6 z0.025(!s2) (Hedges et al. 1999). To explain variation in pigment data, multiple regression models were tested in natural (n 5 29) and restored (n 5 22) data sets from Mission Bay using salinity, sand, and organic matter as independent variables. Since water content was very strongly correlated with organic matter in both data sets (r 5 0.78 and 0.73), it was excluded from the analyses; the other three variables were not strongly correlated with each other (20.16 # r # 0.09). To assess the relative strength of environmental factors in the models, the proportion of variability explained by each independent factor was calculated as g2 5 SSfactor/SStotal. All reported errors are 6 1SE unless otherwise noted. RESULTS Spatial Variation in Environmental Conditions At Mission Bay, all four habitat types in natural wetland had very similar pore-water salinity (F3,28 5 0.05, P 5 0.99; Table 1) and sand content (F3,25 5 1.5, P 5 0.25). Sediment water content at low tide, however, differed with habitat (F3,28 5 17.6, P , 0.0001) with more moisture under Spartina and succulent marsh canopies. Differences in water content coincided with a strong gradient in organic matter, increasing from 4–5% in unvegetated habitats to 14% and 38% in Spartina and succulent marsh respectively (F3,26 5 9.8, P , 0.0002). The extent to which environmental conditions in the restored wetland habit were similar to the
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Table 1. Habitat-level and natural versus restored differences in wetland sediment variables in Mission Bay. Data in means 6 SE (n). Letters indicate statistical differences among wetland habitats in the natural marsh (Fisher’s LSD test at a 5 0.05). MUD 5 mudflat; CRK 5 creek-banks; SPAR 5 Spartina marsh; SUCC 5 succulent marsh; NA 5 not applicable. Habitat Natural wetland
Restored wetland
MUD CRK SPAR SUCC MUD CRK SPAR SUCC
Salinity (psu) 6 1.6 6 2.4 6 1.5 6 2.0 NA 41.9 6 1.4 42.5 6 1.1 55.9 6 5.6 41.8 41.9 42.4 42.7
(8)a (8)a (8)a (8)a (8) (8) (8)
Water (g g21) 6 0.03 6 0.04 6 0.04 6 0.03 NA 0.45 6 0.05 0.45 6 0.03 0.30 6 0.02 0.48 0.52 0.67 0.82
natural site depended on habitat type. Overall, water, pore-water salinity and sediment organic content in restored creek-banks were very similar to the natural site (all F1,14 # 1.7, P $ 0.2). Restored creeks were about 1.5 times sandier (F1,14 5 7.8, P 5 0.015). Pore water salinity in restored Spartina marsh was also similar to natural wetland (F1,14 5 0.002, P 5 0.96). However, restored sediments were twice as sandy as natural habitat (F1,13 5 26.5, P 5 0.0002), less enriched in organic matter (F1,13 5 6.0, P 5 0.029), and retained less water at low tide (F1,14 5 21.6, P 5 0.0004). Restored Spartina densities (286 6 55, n 5 8) were 34% lower than natural wetland density (435 6 129, n 5 5), but variable (F1,11 5 1.5, P , 0.25). Light transmission was similar through natural (35 6 8%; n 5 3) and restored (37 6 9%; n 5 5) marsh canopies. Environmental differences between the natural and restored site were greatest in upper intertidal succulent marsh. Pore water salinities were elevated (F1,14 5 5.0, P 5 0.042) and water content was nearly three times lower at the restored site (F1,14 5 185, P , 0.0001). Restored sediments were also nearly twice as sandy (F1,10 5 10.6, P 5 0.009) and had 19 times less organic matter (F1,11 5 13.0, P 5 0.004). Some of the sediment differences in succulent marsh may have been due to lower restored marsh plant abundance as reflected in higher light transmission to the sediment surface (natural site: 13 6 8% [n 5 4]; restored site: 59 6 24% [n 5 2]).
Sand (g g21) 6 0.08 6 0.09 6 0.05 6 0.12 NA 0.82 6 0.03 0.68 6 0.05 0.81 6 0.05
(8)a (8)a (8)b (8)c
0.47 0.56 0.34 0.44
(8) (8) (8)
Organics (g g21) 6 0.01 6 0.01 6 0.04 6 0.11 NA 0.05 6 0.03 0.05 6 0.01 0.02 6 0.01
(8)ab (8)a (8)b (5)ab
0.04 0.05 0.14 0.38
(8) (7) (7)
(8)a (8)a (8)a (6)b (8) (7) (7)
At Tijuana Estuary, sediments in natural Spartina marsh and natural mudflat had very similar water content (F1,22 5 0.1, P 5 0.73), but mudflat sediments were somewhat more saline (F1,19 5 3.4, P 5 0.08; Table 2). Restored mudflat salinities differed little from natural mudflat, (F1,20 5 0.9, P 5 0.34), but restored sediments retained more water at low tide (F1,22 5 12.3, P 5 0.002). Sediments in restored marsh were also wetter (F1,22 5 9.1, P 5 0.006) and more saline (F1,18 5 40.9, P , 0.0001). Spartina densities were very similar between restored (137.1 6 13.1 plants m22) and natural (146.5 6 25.1 plants m22) marsh (F1,20 5 0.1, P 5 0.74). Microphytobenthic Biomass in Natural Wetlands At Mission Bay, chlorophyll a differed significantly among habitats (F3,28 5 3.3, P 5 0.035, v2 5 0.18; Table 3). Mudflats hosted the lowest concentrations (5.6 mg cm22) with significantly higher chlorophyll a in creeks, Spartina marsh, and upper intertidal marsh. At Tijuana Estuary, patterns were reversed: sediment chlorophyll a concentrations were twice as high in mudflat as in Spartina marsh (F1,22 5 3.5, P 5 0.08, v2 5 0.09; Table 4). Composition and Diversity in Natural Wetlands Overall, bacteriochlorophyll a concentrations were 1–2 orders of magnitude smaller than chlorophyll
Table 2. Habitat-level and natural versus restored differences in wetland environmental variables at Tijuana Estuary. Habitat notation follows Table 1. Habitat Natural wetland Restored wetland
MUD SPAR MUD SPAR
Salinity (psu) 55.5 45.5 60.6 82.1
6 6 6 6
4.9 1.7 2.0 5.5
(11)a (10)a (11) (10)
Water (g g21) 0.38 0.40 0.54 0.55
6 6 6 6
0.04 0.04 0.03 0.03
(12)a (12)a (12) (12)
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Table 3. Pigment concentrations in Mission Bay sediments. Data in means 6 SE (all n 5 8). Letters indicate statistical differences among natural wetland habitats (Fisher’s LSD test at a 5 0.05). Habitat notation follows Table 1. NA 5 not applicable. Pigment Concentration (mg cm22)
Natural wetland
Restored wetland
Habitat
Chlorophyll a
Bacteriochlorophyll a
Fucoxanthin
Zeaxanthin
Lutein
MUD CRK SPAR SUCC MUD CRK SPAR SUCC
5.61 6 1.24 7.63 6 1.64b 6.64 6 1.15b 14.28 6 3.62b NA 8.55 6 0.98 3.29 6 0.74 3.74 6 0.79
6 0.01 6 0.02a 6 0.28b 6 0.14b NA 0.31 6 0.12 0.10 6 0.02 0.05 6 0.02
6 0.64 6 0.68a 6 0.54a 6 1.04a NA 4.25 6 0.83 2.63 6 0.97 2.33 6 0.56
6 0.04 6 0.06a 6 0.14ab 6 0.27b NA 0.34 6 0.07 0.27 6 0.04 0.16 6 0.03
6 0.04a 6 0.05a 6 0.07a 6 0.04a NA 0.14 6 0.06 0.13 6 0.04 0.03 6 0.01
a
a
0.03 0.05 0.55 0.55
2.75 3.48 3.38 4.22
a
0.23 0.24 0.50 0.94
0.14 0.15 0.23 0.16
significantly between habitats (F1,13 5 0.3, P 5 0.58, v2 < 0.00; Table 4); bacteriochlorophyll a/chlorophyll a ratios were also similar (F1,13 5 0.6, P 5 0.44, v2 < 0.00). Zeaxanthin and lutein differed little between habitats (F1,22 5 1.6, P 5 0.22, v2 5 0.02 and F1,22 5 0.8, P 5 0.31, v2 < 0.00, respectively). However, there was a twofold increase in fucoxanthin in mudflats (F1,22 5 4.4, P 5 0.049, v2 5 0.12). Patterns of individual pigment abundance resulted in similar zeaxanthin/fucoxanthin ratios (F1,22 5 0.2, P 5 0.68, v2 < 0.00) and diversity among habitats (and F1,13 5 1.3, P 5 0.28, v2 5 0.02).
a across natural habitats at Mission Bay. Spartina and succulent marshes supported 10 times more bacteriochlorophyll a than unvegetated creek-banks and 18 times more pigment than mudflat (F3,28 5 3.5, P 5 0.029, v2 5 0.19; Table 3). Bacteriochlorophyll a/chlorophyll a ratios (which estimate the relative biomass of anoxygenic versus oxygenic primary producers) also varied more than tenfold among habitats (F3,28 5 2.7, P 5 0.06, v2 5 0.27), with the highest ratios in vegetated marshes (Figure 1A). Zeaxanthin concentrations were several times higher in vegetated marshes than in mudflat or creek-bank sediment (F3,28 5 4.7, P 5 0.009, v2 5 0.26). In contrast, fucoxanthin (F3,28 5 0.7, P 5 0.55, v2 < 0.00) and lutein (F3,28 5 0.7, P 5 0.57, v2 < 0.00) differed little among habitats. These patterns led to habitat-level variation in zeaxanthin/fucoxanthin ratios (F3,28 5 3.1, P 5 0.044, v2 5 0.16; Figure 1B) with marshes generally showing about a 2-fold enrichment in zeaxanthin relative to unvegetated habitat. Taxonomic diversity in Mission Bay was highest in succulent marsh and lowest in creek-banks and mudflat (F3,28 5 3.5, P 5 0.028, v2 5 0.19; Figure 1C). At Tijuana Estuary, bacteriochlorophyll a concentrations (which, like Mission Bay, were two orders of magnitude smaller than chlorophyll a) did not differ
Table 4. Table 1.
a
Restored Wetland Assemblages Microphytobenthic assemblages in restored wetland sediments were compared to natural communities for each habitat type (Figure 2). In Mission Bay, natural and restored creek-banks were similar with respect to chlorophyll a, fucoxanthin, zeaxanthin, lutein, zeaxanthin/fucoxanthin ratios, and diversity (all F1,14 # 1.9, P $ 0.19; Tables 3,4). Restored creek-banks were enriched in bacteriochlorophyll a (F1,14 5 4.5, P 5 0.053) and had higher bacteriochlorophyll a/chlorophyll a ratios (F1,14 5 8.2, P 5 0.013) than natural creeks. Natural Spartina marsh in Mission Bay contained twice as much chlorophyll a as restored marsh (F1,14
Pigment concentrations in Tijuana Estuary sediments. Data in means 6 SE (n). Habitat notation follows Pigment Concentration (mg cm22) Habitat
Natural wetland Restored wetland
MUD SPAR MUD SPAR
Chlorophyll a 14.40 6.71 10.75 9.46
6 6 6 6
3.95 1.21 1.14 1.52
Bacteriochl a a
(12) (12)b (12) (12)
0.06 0.08 0.26 0.26
6 6 6 6
0.02 0.03 0.06 0.07
Fucoxanthin a
(9) (6)a (5) (6)
4.82 2.48 5.38 5.09
6 6 6 6
1.01 0.48 0.55 0.91
Zeaxanthin a
(12) (12)b (12) (12)
0.84 0.52 0.80 0.55
6 6 6 6
0.23 0.12 0.08 0.10
Lutein a
(12) (12)a (12) (10)
0.54 0.37 0.54 0.25
6 6 6 6
0.15 0.10 0.10 0.06
(12)a (12)a (12) (10)
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5 6.0, P 5 0.028); there was also a trend towards higher bacteriochlorophyll a (F1,14 5 2.6, P 5 0.13) and more zeaxanthin (F1,14 5 2.8, P 5 0.12) within natural sediments, but replicate samples showed high variability. Natural versus restored differences in fucoxanthin, lutein, bacteriochlorophyll a/chlorophyll a, zeaxanthin/fucoxanthin, and taxonomic diversity were small (all F1,14 # 1.6, all P $ 0.22). The greatest differences in community composition between natural and restored sites in Mission Bay were observed in upper intertidal succulent marsh. Natural chlorophyll a concentrations were about 4 times higher (F1,14 5 8.1, P 5 0.01), and bacteriochlorophyll a levels were 11 times higher (F1,14 5 11.8, P 5 0.004), leaving the natural site more enriched in pigment from anoxygenic producers (bacteriochlorophyll a/chlorophyll a difference: F1,14 5 5.5, P 5 0.04). Fucoxanthin (F1,14 5 3.0, P 5 0.11), lutein (F1,14 5 10.8, P 5 0.005), and zeaxanthin (F1,14 5 8.5, P 5 0.01) concentrations were also higher in natural wetland. Significant differences in zeaxanthin/fucoxanthin (F1,14 5 5.5, P 5 0.03) and diversity (F1,14 5 10.0, P 5 0.007) implied shifts in taxon dominance (Table 3, Figure 1). In mudflats at Tijuana Estuary, only bacteriochlorophyll a and bacteriochlorophyll a/chlorophyll a ratios differed markedly between natural and restored areas (F1,12 5 14.0, P 5 0.003 and F1,12 5 9.7, P 5 0.009). All other pigment measures were similar (all F , 2.0, all P . 0.2; Table 3; Figure 2). Restored Spartina marsh sediments had 3 times more bacteriochlorophyll a (F1,10 5 5.5, P 5 0.04), 2 times more fucoxanthin (F1,22 5 6.4, P 5 0.02), and lower zeaxanthin/fucoxanthin ratios (F1,20 5 3.3, P 5 0.09) than natural marsh. Sites were similar with respect to chlorophyll a (F1,22 5 2.0, P 5 0.17), bacteriochlorophyll a/chlorophyll a ratios (F1,10 5 2.0, P 5 0.19), zeaxanthin (F1,20 5 0.04, P 5 0.8), lutein (F1,20 5 1.0, P 5 0.32), and diversity (F1,10 5 1.0, P 5 0.33). Figure 1. Habitat-level differences in A) bacteriochlorophyll a/chlorophyll a ratios, B) zeaxanthin/fucoxanthin ratios, and C) taxonomic diversity in sediments from Mission Bay (left panels) and Tijuana Estuary (right panels). Data are means 6 1 SE. Habitats are generally located at increasing tidal elevation from left to right within each site. MUD 5 mudflat; CRK 5 creek-bank; SPAR 5 Spartina marsh; SUCC 5 high intertidal succulent marsh; CHL A 5 chlorophyll a; BCHL A 5 bacteriochlorophyll a; ZEAX 5 zeaxanthin; FUCO 5 fucoxanthin.
Microphytobenthic Composition and Environmental Variables Sediment sand, organic matter, and pore water salinity relationships with community structure were tested with multiple regression among Mission Bay samples. At the natural site, a significant portion of variation in bacteriochlorophyll a (R2 5 0.34, P 5 0.01) and bacteriochlorophyll a/chlorophyll a ratios (R2 5 0.29, P 5 0.03) was explained by the models, with organic matter being positively correlated with both pigment measures (g2 5 0.29, F1,25 5 10.9, P 5 0.003, and g2 5 0.27, F1,25 5 9.5, P 5 0.005
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Figure 2. Natural versus restored differences in microphytobenthic pigments represented as effect size estimates (Hedges’ response ratios 6 95% confidence intervals). A) creek-banks (Mission Bay) or mudflat (Tijuana Estuary), B) Spartina salt marsh, and C) upper intertidal succulent marsh. Positive effect sizes indicate greater pigment biomass (or larger values of community metrics) in the restored wetland. CHL A 5 chlorophyll a; BCHL A 5 bacteriochlorophyll a; ZEAX 5 zeaxanthin; FUCO 5 fucoxanthin.
respectively). Sand and salinity appeared to explain little variability (all g2 # 0.05). Overall models for chlorophyll a, fucoxanthin, zeaxanthin, lutein, zeaxanthin/fucoxanthin ratios, and diversity were not significant (all R2 , 0.23, all P . 0.11). However, organic matter was modestly related (positively) to zeaxanthin (g2 5 0.13, F1,25 5 4.1, P 5 0.05) and diversity (g2 5 0.17, F1,25 5 5.3, P 5 0.03). For all other independent variables, g2 # 0.10. At the restored site, variation in bacteriochlorophyll a and bacteriochlorophyll a/chlorophyll a
ratios was partially explained by model variables (R2 5 0.29, P 5 0.10 and R2 5 0.42, P 5 0.02, respectively) with organic matter accounting for the majority of pigment variation (g2 5 0.28, F1,18 5 7.0, P 5 0.02 and g2 5 0.37, F1,18 5 11.4, P 5 0.003). Organic matter was also positively associated with zeaxanthin concentration (g2 5 0.17, F1,18 5 3.9, P 5 0.06). Very little variation in chlorophyll a, fucoxanthin, or lutein was explained in the full models (all R2 , 0.1); models for zeaxanthin/ fucoxanthin and diversity (both R2 5 0.16) were also not significant.
Janousek, MICROPHYTOBENTHIC DIVERSITY IN MARINE WETLANDS Because of the strong association between sediment organic matter and vegetation presence in Mission Bay, I attempted to separate light effects from variation in organic matter by pooling and reanalyzing samples from similar light environments. In low light environments (i.e., marshes; n 5 21), organic matter was still positively correlated with bacteriochlorophyll a (r 5 0.45, P 5 0.04) and bacteriochlorophyll a/chlorophyll a (r 5 0.47, P 5 0.03), but was more weakly correlated with zeaxanthin (r 5 0.26, P 5 0.26) and zeaxanthin/fucoxanthin (r 5 0.22, P 5 0.33). In assemblages from higher light environments (mudflat and creek-banks; n 5 24), organic matter was also strongly correlated with bacteriochlorophyll a (r 5 0.44, P 5 0.03), bacteriochlorophyll a/chlorophyll a (r 5 0.45, P 5 0.03), and zeaxanthin (r 5 0.37, P 5 0.07), but not with zeaxanthin/fucoxanthin (r 5 0.08, P 5 0.70). DISCUSSION Pigment and abiotic data provided insight into habitat-level differences in microphytobenthic composition and environmental co-variation with community structure. In Mission Bay, there were distinct compositional shifts between habitats, from diatomdominated sediments in unvegetated wetland to sediments richer in cyanobacteria and anoxygenic phototrophic bacteria in marsh habitat. Organic matter, either directly or indirectly by contributing to benthic anoxia, appeared to play a strong role in compositional heterogeneity over space; algal community structure was largely independent of sediment sand content and salinity. Less pronounced differences in community structure were evident at Tijuana Estuary. Overall, the existence of spatial heterogeneity in composition has implications for understanding spatial variability in ecosystem function within natural wetlands, and evaluation of wetland restoration efforts. Habitat-level Variation in Natural Wetlands At Mission Bay, intertidal habitats clearly differed in microphytobenthic community structure. Vegetated habitat appeared to host higher total algal biomass (chlorophyll a) and more cyanobacteria and anoxygenic phototrophic bacteria. Although individual pigment data might indicate habitat-linked changes in carbon to pigment ratios (because of light differences, for example), pigment ratio data suggests actual shifts in the relative abundance of major groups between habitats, coinciding with the presence or absence of a vascular plant canopy. Anoxygenic purple bacteria and cyanobacteria made
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up a larger fraction of primary producer biomass in (particularly) the succulent marsh. This increase in taxon evenness drove differences in diversity (Figure 1C). With respect to cyanobacteria, these habitat-level data seem to follow patterns in other intertidal wetland systems. For example, Brotas and PlanteCuny (1998) noted higher zeaxanthin concentrations in salt marsh than in mudflat and Al-Zaidan et al. (2006) found increasing cyanobacterial abundance with tidal height. In Mission Bay, there was also a pronounced intertidal gradient in anoxygenic phototrophic bacteria. These organisms clearly showed increased abundance in Spartina and halophyte marsh in Mission Bay; however, at Tijuana Estuary, they were about equally abundant in Spartina marsh and mudflat. Although some studies suggest that bacteriochlorophyll-containing prokaryotes can be abundant in sediment from coastal sites in southern and Baja California (Armitage and Fong 2004, Ley et al. 2006), their natural history is poorly understood. Habitat-level differences in microphytobenthic communities observed at Mission Bay were likely driven by variation in sediment organic matter (or, more directly, by sediment anoxia). Spartina-dominated and succulent marshes had several fold higher organic matter than unvegetated habitats and both hosted larger absolute and relative concentrations of pigment from anoxygenic producers. Multiple regression models in natural and restored sites supported these general patterns: there was a moderately strong positive relationship between organic matter and bacteriochlorophyll a and bacteriochlorophyll a/chlorophyll a ratios, but other model variables (sand, salinity) usually accounted for much less variation in the data sets. Putative organic matter effects on community composition appeared to be strongest for anoxygenic producers, but were moderate for cyanobacteria. In these wetlands, variation in organic matter also coincided with differences in sediment water content and vegetation cover. High concentrations of organic matter and water in vegetated habitat probably led to reduced oxygen concentrations in surface sediments, perhaps providing favorable conditions for anoxygenic photobacteria by shifting the oxic/anoxic boundary in the sediment profile towards the surface where more light is available. Data from Tijuana Estuary also suggest that sediment water content may affect anoxygenic producers: the concentration of bacteriochlorophyll a was several times higher in restored wetland, which had elevated water content in both marsh and mudflat. In fact, observed patterns of anoxygenic photobacterial abundance in relation to patches of
172 organic matter or hypoxia may strengthen in summer or fall months (as opposed to the early spring sampling here) because oxygen concentrations are likely to decrease further as organic-rich sediments experience increased heterotrophic microbial activity. Few data exist linking photosynthetic prokaryote abundance to bulk organic matter in coastal wetlands. However, Paterek and Paynter (1988) isolated anoxygenic producers from high intertidal Spartina alterniflora marsh in Georgia but not from creek-side sediments. Guyoneaud et al. (1996) also obtained various species of sulfur and non-sulfur purple photosynthetic bacteria at several organic rich sites in coastal France. Vegetated and unvegetated landscapes also differ in ambient light transmission that might affect algal biomass and composition. However, the role of light intensity in shaping microphytobenthic community structure is not clear. In a Delaware salt marsh, cyanobacteria appeared to respond favorably to higher irradiance generated from canopy removal (Sullivan 1976), however, a cyanobacterial ‘‘bloom’’ failed to appear in a similar experiment conducted in Mississippi (Sullivan 1981). Whitcraft and Levin (2007) found about a twofold reduction in fucoxanthin abundance upon removal of a Salicornia virginica canopy in southern California (this difference might be caused by changes in pigment to biomass ratios, and not necessarily by changes in biomass), but little change in fucoxanthin concentrations when a Spartina foliosa canopy was removed. At Mission Bay, light flux through plant canopies had only a weak or moderate relationship with most pigment measures (|r| # 0.30) except for zeaxanthin/fucoxanthin ratios (r 5 20.39) and taxonomic diversity (r 5 20.40). Above-ground canopies may only partially determine incident light levels for microphytobenthic cells because many diatoms are capable of vertical migration in sediments (Pinckney et al. 1994). Sediment sand content and pore water salinity generally showed little relationship with measures of community structure. Salinity is a highly variable feature of southern California coastal wetlands that can vary with pulses of freshwater input, diurnal tidal cycles, and season. Other studies suggest that diatoms appear to show some preference for finergrained sediment particles (Lucas and Holligan 1999, Waterman et al. 1999), but this association was not evident in Mission Bay. Restored Wetland Assemblages In Mission Bay, differences in microphytobenthic community structure between restored and natural
WETLANDS, Volume 29, No. 1, 2009 sites depended on habitat type. In lower intertidal habitats (creek-banks and Spartina marsh), restored composition generally resembled that of natural habitat, but creeks in the restored site had elevated levels of bacteriochlorophyll a. This difference may be linked to poor oxygenation of sediments along the single main intertidal channel that feeds the restored site (especially near the creek terminus), instead of organic matter content, which did not differ between restored and natural creeks. The largest natural-restored differences in microphytobenthic composition were seen in upper intertidal succulent marsh at Mission Bay (Figure 2). Sediments in this habitat at the restored site were sandy, dry, contained little organic matter, and received increased light because of more open plant canopies. These strong abiotic differences coincided with markedly different microphytobenthic communities, low in overall abundance and taxonomic diversity and with less bacteriochlorophyll a and smaller bacteriochlorophyll a/chlorophyll a ratios. Levin and Talley (2002) also noted a lack of organic matter in vegetated habitat at this site. Low organic matter content in restored wetlands (persisting for up to several decades) appears to be common to coastal rehabilitation efforts (Craft et al. 1988, Moy and Levin 1991, Edwards and Proffitt 2003), and it may result in long-term effects on ratios of microphytobenthic groups. At Tijuana Estuary, natural versus restored differences in community structure were not very pronounced in mudflat or Spartina marsh, coinciding with the rapid development of microphytobenthos at this restored site (Janousek et al. 2007). Bacteriochlorophyll a was elevated in restored habitats, however, possibly implicating hydrologic or sediment differences for this disparity. Sediments in restored habitat at Tijuana Estuary may have been more anoxic than the natural habitat since the large restoration area was hydrologically connected to natural habitat by only a single intertidal channel and artificially constructed secondary channels that may not have provided adequate drainage. Anoxygenic producers may also have appeared to be higher in restored wetland if natural wetland populations resided deeper in sediment layers than sampled (due possibly to sandier sediments and deeper light penetration). CONCLUSIONS Pigment data from these southern California wetlands show spatial variation in microphytobenthic community structure with several important ecological and management implications. First,
Janousek, MICROPHYTOBENTHIC DIVERSITY IN MARINE WETLANDS despite their ubiquity in sedimentary habitats, microphytobenthic taxa can differ in their evenness across coastal wetland habitats. Diatoms are consistently present as major components of these southern California tidal wetlands (see also Armitage and Fong 2004) and appear to be broadly tolerant of a range of sediment characteristics (Larson and Sundba¨ck 2008). Cyanobacteria and anoxygenic phototrophic bacteria are generally less abundant, but are more important components of some vegetated habitats. Perhaps less broadly tolerant than diatoms, their abundance may be driven more strongly by particular sediment features such as organic matter. Second, because microphytobenthic composition can exhibit distinct spatial heterogeneity at high taxonomic levels, it is important to determine whether or not this variation affects important ecosystem functions such as primary production, nutrient cycling, and contributions to food webs. Localized patches of higher abundance of cyanobacteria and anoxygenic phototrophs, for example, may be characterized by increased sulfide oxidation or nitrogen fixation. Additionally, spatial differences in microphytobenthic composition may directly affect wetland consumers that specialize on particular microphytobenthic taxa (Decho and Castenholz 1986, Buffan-Dubau et al. 1996). To further understanding of the important wetland processes mediated by microphytobenthos, it is necessary for ecologists to move beyond aggregate measures of microproducer communities (e.g., chlorophyll a) towards characterization of composition. Lastly, data from Mission Bay suggest that wetland habitats may differ in the rate of microphytobenthic succession. Higher intertidal habitats with less frequent tidal inundation may recover more slowly than habitats at lower elevation. Ecologists should carefully evaluate all landscapes present in restoration efforts to test their equivalency with natural habitat. For southern California in particular, because succulent marsh is an important marsh type across the region, restoration efforts need to ensure the success of this particular habitat. ACKNOWLEDGEMENTS Field work was conducted at the University of California Natural Reserve System’s Kendall-Frost Mission Bay Marsh Reserve (UCSD), the Northern Wildlife Preserve and Crown Point Mitigation Site (City of San Diego), and the Tijuana Estuary National Estuarine Research Reserve. This study was supported by funding from a Mildred E. Mathias Graduate Student Research Grant from
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the UC Natural Reserve System, NOAA CICEET grant NA97OR0338, Achievement Rewards for College Scientists (Los Angeles chapter), the graduate department at Scripps Institution of Oceanography, and the California Department of Boating and Waterways. I thank N. Ben-Aderet, J. Fodrie, E. Green, J. Leddick, L. Levin, L. Pierotti, M. Vernet, and others for assistance. D. Holway, L. Levin, N. Knowlton, M. Vernet and anonymous individuals kindly reviewed previous versions of the manuscript. LITERATURE CITED Al-Zaidan, A. S. Y., H. Kennedy, D. A. Jones, and S. Y. AlMohanna. 2006. Role of microbial mats in Sulaibikhat Bay (Kuwait) mudflat food webs: evidence from d13C analysis. Marine Ecology Progress Series 308:27–36. Armitage, A. R. and P. Fong. 2004. Upward cascading effects of nutrients: shifts in a benthic microalgal community and a negative herbivore response. Oecologia 139:560–67. Austen, I., T. J. Anderson, and K. Edelvang. 1999. The influence of benthic diatoms and invertebrates on the erodibility of an intertidal mudflat, the Danish Wadden Sea. Estuarine Coastal and Shelf Science 49:99–111. Brotas, V., T. Cabrita, A. Portugal, J. Sero ˆ dio, and F. Catarino. 1995. Spatio-temporal distribution of the microphytobenthic biomass in intertidal flats of Tagus Estuary (Portugal). Hydrobiologia 300/301:93–104. Brotas, V. and M-R. Plante-Cuny. 1996. Identification et quantification des pigments chlorophylliens et carote´noı¨des des se´diments marins: un protocole d’analyse par HPLC. Oceanologica Acta 19:623–34. Brotas, V. and M-R. Plante-Cuny. 1998. Spatial and temporal patterns of microphytobenthic taxa of estuarine tidal flats in the Tagus Estuary (Portugal) using pigment analysis by HPLC. Marine Ecology Progress Series 171:43–57. Brotas, V. and M-R. Plante-Cuny. 2003. The use of HPLC pigment analysis to study microphytobenthos communities. Acta Oecologica 24:S109–S115. Buffan-Dubau, E., R. de Wit, and J. Castel. 1996. Feeding selectivity of the harpacticoid copepod Canuella perplexa in benthic muddy environments demonstrated by HPLC analysis of chlorin and carotenoid pigments. Marine Ecology Progress Series 137:71–82. Callaway, R. M. and S. C. Pennings. 2000. Facilitation may buffer competitive effects: indirect and diffuse interactions among salt marsh plants. American Naturalist 156:416–24. Carpenter, E. J., C. D. Van Raalte, and I. Valiela. 1978. Nitrogen fixation by algae in a Massachusetts salt marsh. Limnology and Oceanography 23:318–27. Carver, R. E. 1971. Procedures in Sedimentary Petrology. Wiley & Sons, Inc., New York, NY, USA. Craft, C. B., S. W. Broome, and E. D. Seneca. 1988. Nitrogen, phosphorus and organic carbon pools in natural and transplanted marsh soils. Estuaries 11:272–80. Currin, C. A. and H. W. Paerl. 1998. Environmental and physiological controls on diel patterns of N2 fixation in epiphytic cyanobacterial communities. Microbial Ecology 35:34–45. Decho, A. W. and R. W. Castenholz. 1986. Spatial patterns and feeding of meiobenthic harpacticoid copepods in relation to resident microbial flora. Hydrobiologia 131:87–96. Edwards, K. R. and C. E. Proffitt. 2003. Comparison of wetland structural characteristics between created and natural salt marshes in southwest Louisiana, USA. Wetlands 23:344–56. Falkowski, P. G. and J. LaRoche. 1991. Acclimation to spectral irradiance in algae. Journal of Phycology 27:8–14.
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