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CHAPTER EIGHT

ESTUARINE BENTHIC ALGAEKaren J. McGlathery, Kristina Sundback, and Peggy Fong

8.1 INTRODUCTIONBenthic algae play a key role in regulating carbon andnutrient turnover and in supporting food webs inshallow-water coastal environments. They are espe-cially important in the wide diversity of estuarinehabitats found worldwide. Benthic producers are gen-erally divided into macroalgae and microalgae (alsoknown as microphytobenthos). Macroalgae contributebetween 4.8% and 5.9% of the total marine net primaryproductivity (calculated from Duarte and Cebrian,1996). Although lower than total oceanic (81.1%) andcoastal (8.5%) phytoplankton, the local macroalgalproductivity (per square meter) is comparable to someof the most productive terrestrial ecosystems such astropical forests. Benthic microalgae often form visiblebrown or green mats on the sediment surface. Thesemats are thin, as the microalgae are confined to thephotic zone (1–3 mm) of the sediment, yet the densityof algae and other microorganisms is usually high,often 100–1000 times higher than in the water column.In shallow estuaries, benthic microalgae normallyaccount for 20–50% of the total primary production(Underwood and Kromkamp, 1999). In this chapter,we discuss the benthic algal communities that inhabitthe soft-bottom (mud/sandflat, seagrass bed, marsh),hard-bottom (rocky intertidal, shallow subtidal), andcoral reef habitats that lie within estuarine ecosys-tems.

Estuarine Ecology, Second Edition. Edited by John W. Day, Jr., Byron C. Crump, W. Michael Kemp, and Alejandro Yanez-Arancibia. 2013 Wiley-Blackwell. Published 2013 by John Wiley & Sons, Inc.

8.2 TAXONOMYAll algae at some stage of their life cycles are unicellu-lar (usually as reproductive stages such as spores orzygotes), and they are viewed as ‘‘primitive’’ photo-synthetic organisms because of their relatively simpleconstruction and their long evolutionary history.Prokaryotic ‘‘blue-green algae,’’ or cyanobacteria, arethe oldest group, with fossils dating back almost 3000million years. These first algal fossil remains includestromatolites, which are structures formed in shallowtropical waters when cyanobacterial mats accretelayers by trapping, binding, and cementing sedimentgrains. Photosynthesis by these early primaryproducers was responsible for much of the oxygenthat eventually built up to the levels that occurtoday. Evolution of eukaryotic algae occurred muchlater, about 700–800 million years ago, althoughthis date is difficult to determine more exactly asmost groups were composed of soft tissue thatwould not have been preserved reliably in the fossilrecord.

Marine macroalgae or ‘‘seaweeds’’ are a func-tional rather than phylogenetic group comprisingmembers from two kingdoms and at least four majorphyla (divisions). There is a wide variation in algalclassification schemes among systematists, but thetraditional divisions for macroalgae are Cyanobacteria(prokaryotic blue-green algae, sometimes termed

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Cyanophyta), Chlorophyta (green algae), Phaeophyta(brown algae), and Rhodophyta (red algae) (Littler andLittler, 2000).

Marine green algae range from cold temperateto tropical waters. Green algae reach highest diver-sity and abundance in tropical regions, with severalfamilies such as the Caulerpaceae and Udoteaceae beingvery abundant in coral reef and associated seagrasshabitats. Often overlooked, but very abundant, arefilamentous green algae that bore into coral skeletonand proliferate widely, with high rates of produc-tivity (Littler and Littler, 1988). Opportunistic greenalgae form nuisance blooms in estuaries worldwide;in eutrophic systems, they form almost monospecificmats of extremely high biomass.

Brown algae are almost exclusively marine andare dominant in temperate waters where hard-bottomed habitats occur. Some genera of structurallyrobust forms such as Laminaria and Sargassumdominate in very high energy zones. Kelps are‘‘ecoengineers’’ that form extensive forests in coastalareas where nutrients are supplied by upwelling.Other groups of fast growing and more opportunisticgenera such as Dictyota may form seasonal blooms intropical and subtropical regions.

The majority of seaweed species is in theRhodophyta. At present, the approximately 4000named species of red algae exceed the number ofspecies in all other groups combined (Lee, 1999).Although red algae are extremely speciose in tropicaland subtropical regions, their biomass is low relativeto that in temperate areas. The most common forms ofred algae in the tropics include crustose members ofthe family Corallinaceae as well as a high diversity ofsmall, less obvious filamentous species that comprisealgal turfs. However, there are some genera ofupright and branching calcifying forms such asGalaxaura and branching or flattened foliose red algaein the genera Laurencia, Asparagopsis, and Halymeniathat can be quite conspicuous and abundant on reefsunder certain conditions. The highest biomass of redalgae is found in temperate and boreal regions. Somelarge fleshy members of the Rhodophyta with descrip-tive names such as ‘‘Turkish towels’’ blanket rockyintertidal and subtidal regions. Other genera, such asGracilaria, form blooms in estuaries and lagoons.

In most cases, the benthic microalgal communityin estuarine habitats is a mixture of several taxonomi-cal groups, although blooms tend to be dominated byone or few species. The taxa that form typical visiblemicrobial mats on the sediment surface in the photiczone are mostly diatoms (phylum Bacillariophyta) andcyanobacteria (the prokaryotic phylum Cyanophytaor Cyanobacteria). The term microbial mat originally

referred to consortia dominated by prokaryotic pho-totrophs (Stal and Caumette, 1992), but here it isused in a broader sense, including all types of matsconsisting of microscopic phototrophic organisms.

Diatoms are by far the most common taxonomicgroup, giving the sediment a brown color becauseof the pigment fucoxanthin. Benthic diatoms are dif-ferent from planktonic diatoms in that they mostlyrepresent the pennate diatoms, with more or lessbilateral symmetry (classes Fragilariophyceae and Bacil-lariophyceae; according to the systematics in Roundet al., 1990). They are solitary, and when they havea raphe (a slitlike structure) on both valves of theirsilica frustule (or covering), they are motile. Thosethat have no raphe, or a raphe only on one valve,can form short colonies. Some centric diatoms (classCoscinodiscophyceae) can be common on sediments, forexample, Paralia sulcata. The size of benthic diatomsranges from a few micron to 500 µm; the sigmoidcells belonging to the genera Gyrosigma and Pleu-rosigma are some of the largest. Because many benthicdiatoms are small (<10 µm), it is difficult to identifylive cells to species level in a light microscope. Whenthe organic cell contents are removed by oxidation toprepare ‘‘diatom slides,’’ the taxonomically importantornamentation of the silica frustule can be viewed.

Cyanobacteria are widespread both on soft andhard substrates. They form mats along reef marginsor on coral (Smith et al., 2009), may be epiphytic onother algae (Fong et al., 2006), rapidly colonize openspace opportunistically after disturbances (Belk andBelk, 1975), and may bloom in response to nutrientenrichment (Armitage and Fong, 2004). Cyanobac-terial mats are also common on salt marshes, par-ticularly in subtropical and tropical estuaries andextreme habitats such as hypersaline lagoons. Theyare laminated systems that form interdependent lay-ers of vertically stratified phototrophic, heterotrophic,and chemotrophic microorganisms. They function aslaterally compressed ecosystems that support mostof the major biochemical cycles within a verticaldimension of a few millimeters (Paerl and Pinckney,1996). Typical benthic genera are the filament-formingOscillatoria and Microcoleus and the colony-formingMerismopedia. Many filamentous benthic cyanobacte-ria fix nitrogen gas (N2) (Paerl and Pinckney, 1996).See Chapter 4.

Flagellates such as dinoflagellates (Dinophyta),euglenophytes (Euglenophyta), chlorophytes (Chloro-phyta), and cryptophytes (Cryptophyta) are also foundin estuarine microphytobenthos. Dense populationsof dinoflagellates of the genus Amphidinium canoccasionally give the sediment surface a red brown

Functional Forms | 205

color. See Chapter 4. As for phytoplankton, pho-topigments can be used to identify and quantify thepresence of major taxonomical groups of benthicmicroalgae in surface sediments (Chapter 4).

8.3 FUNCTIONAL FORMSStructurally, benthic algae include diverse forms thatrange from single cells to giant kelps over 45 m inlength with complex internal structures analogous tovascular plants. Species diversity may be extremelyhigh in benthic algal communities (Guiry and Guiry,2007; see http://www.algaebase.org), and can be sim-plified by classifying algae by functional-form cate-gories. Steneck and Dethier (1994) classified algae intothe following groups based on productivity and sus-ceptibility to grazing: microalgae, filamentous, crus-tose, foliose, corticated foliose, corticated macrophyte,leathery macrophyte, and articulated calcareous.

For macroalgae, a classification scheme based ona broader set of characteristics was put forward byLittler and Littler (1984): sheet, filamentous, coarselybranched, thick leathery, jointed calcareous, and crus-tose forms (Table 8.1). These groups of functionalforms have characteristic rates of nutrient uptakeand mass-specific productivity, turnover rates, andresistance to herbivory that allow them to performsimilarly in response to environmental conditions,despite differences in taxonomy. A key characteristicthat drives these differences in function based on formis the ratio of surface area to volume (SA:V) of the

thallus. Macroalgae are also grouped more generallyinto ‘‘ephemeral’’ or ‘‘perennial’’ forms. Ephemeralmacroalgae typically have a high thallus SA:V andinherently rapid nutrient uptake and growth rates.Most of the bloom-forming macroalgae that occur inresponse to nutrient overenrichment (eutrophication)(e.g., Ulva sp., Chaetomorpha sp., Gracilaria sp., Polysi-phonia sp.) are ephemeral, and usually comprise verysimple thallus forms such as those in the first three cat-egories of Littler and Littler (1984). They tend to livefloating and unattached or loosely attached to hardsurfaces (i.e., shells, worm tubes) on the sediment(Schories and Reise, 1993; Thomsen and McGlath-ery, 2005). Perennial species such as crustose andcalcareous macroalgae tend to live in low nutrientor stressful habitats (e.g., low light, low tempera-ture) where a slow growth rate or perennial life formconfers an advantage.

For benthic microalgae that live in sediments, theenergy regime of the habitat determines the dominantlife forms. In wave-exposed, well-sorted sands, lifeforms that are firmly attached to sand grains dominateand are called epipsammic (attached to sand grains).In high energy sand, most epipsammic diatoms arefound in the crevices of the sand grains, wherethey are protected from abrasion. Typical genera areAchnanthes, Cocconeis (with raphe on one valve), andsmall-sized Navicula-like genera and Amphora (rapheon two valves) (Fig. 8.1a). These life forms attach bymucopolysaccharides extruded through their raphe.In less wave-exposed sands, solitary cells or colonies

TABLE 8.1 Functional-form groups of predominant macroalgae, their characteristics, and representative taxa

Functional-form External Comparative Thallus ExampleGroup Morphology Anatomy Size/texture Genera

1. Sheetlike algae Flattened or thintubular (foliose)

One–several celllayers thick

Soft, flexible UlvaHalymenia

2. Filamentous algae Delicately branched Uniseriate,multiseriate, orlightly corticated

Soft, felxible ChaetomorphaCladophora.GelidiumCaulerpa

3 Coarselybranched algae

Terete, upright,thicker branches

Corticated Wiry to fleshy AcanthophoraLaurencia

4. Thick leatherymacrophytes

Thick blades andbranches

Differentiated,heavilycorticated, thickwalled

Leathery-rubbery SargassumTurbinaria

5. Jointedcalcareousalgae

Articulated,calcareous,upright

Calcified genicula,flexibleintergenicula

stony GalaxauraAmphiroa

6. Crustose algae Epilithic, prostrate,encrusting

Calcified,heterotrichous

Stony and tough PorolithonHydrolithon

Source: Adapted from Littler and Littler (1984).


(a) (b)

FIGURE 8.1 Benthic diatom assemblages viewed by scanning electron microscopy (SEM). (a) Epipsammic diatoms (Achnan-thes and Navicula) in the cavity of a sand grain. (b) Vertical cut of a sediment surface at low tide photographed in a lowtemperature SEM. Motile diatoms have moved to the sediment surface where they form a dense microalgal mat. Stringsforming networklike patterns consist of extracellular polymeric substances (EPS) excreted by diatoms (the pattern is anartifact produced by the method). Source: Photograph (a) by H. Hakansson and K. Sundback, (b) by A. Miles, SedimentEcology Research Group, University of St. Andrews, Scotland.

of small diatoms are found protruding from the sed-iment particles. Such genera include Fragilaria andOpephora, which lack raphe, but attach through amucopolysaccharide pad extruded from apical pores.The more sheltered the sediment is from wave expo-sure, the more common are motile life forms (epipelic;originally meaning ‘‘living on mud’’). These are thediatoms that form visible, cohesive microbial matson the sediment surface, particularly on muddy tidalflats (Fig. 8.1b). The cohesiveness is due to extracellu-lar polymeric substances (EPS) that are extruded fromthe raphe and from pores in the silica frustule. Theproduction of EPS is related to the motility of raphe-bearing life forms (genera such as Navicula, Amphora,Nitszchia, Gyrosigma, etc.; for systematics of the diatomgenera, see Round et al., 1990). In fine sediments,epipsammic life forms are found attached to flocs oforganic matter consisting of detritus and fecal pellets.

8.4 HABITATS8.4.1 Soft-Bottom: Mud/Sandflats,Seagrass Beds, and Marshes

Benthic algae are important members of the pri-mary producer community in shallow soft-sediment

systems worldwide where light penetrates to largeareas of the benthos. In those systems subject to lownitrogen loading rates, macroalgae occur in relativelylow abundance attached to the benthos, are epiphyticon seagrass blades, or form drifting mats. Within trop-ical seagrass beds, calcareous and/or siphonaceousgreen macroalgae such as Halimeda and Caulerpa arecommonly attached to the benthos; calcification andchemical defenses provide protection from most her-bivores. Calcified macroalgae ultimately contributesignificantly to the accumulation and stabilization oftropical sands (MacIntyre et al., 2004). In both tropicaland temperate seagrass beds, macro- and microal-gae attach epiphytically to seagrass blades. Althougheven low abundances of epiphytes can have negativeeffects on seagrasses due to shading and interferencewith gas and nutrient exchange, in seagrass systemswith low nutrient loading and intact herbivore popu-lations epiphyte biomass accumulation is modest andcontributions to food webs are significant (Williamsand Ruckelshaus, 1993). In low nutrient soft-sedimentsystems, drift macroalgae are also present in lowabundance, but are ecologically important as theymay provide protection from predation and aid indispersal of invertebrates and fishes (Salovius et al.,2005; Holmquist, 1994). However, when abundancesincrease, drifting mats can have negative effects on

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their seagrass hosts, reducing density through smoth-ering and shading (Huntington and Boyer, 2008).

Macroalgae can occasionally be abundant inthe lower salt marsh zone in estuaries. Examplesinclude the ephemeral green algae (Blidingia, Rhizo-clonium, and Ulva (including former Enteromorpha)),slow-growing stress tolerant and long-lived brownalgae (Fucus and Ascophyllum), inconspicuous slow-growing red algae (Bostrychia and Caloglossa), andinvasive species (e.g., Gracilaria vermiculophylla).Many macroalgae in the understory of salt marshvegetation are complexed with cyanobacteria anddiatom mats. Productivity of these mixed algalcommunities can be very high, at times equalingor exceeding the productivity of the vascular plantcanopy (Zedler, 1982). When algae are abundant inthe understory of the vascular plant community, theymay affect primary production rates, biogeochemicalcycling, trophic interactions, and environmental con-ditions, such as evapotranspiration, infiltration, andsediment characteristics (Brinkhuis, 1977; Mosemanet al., 2004; Boyer and Fong, 2005; Thomsen et al.,2009).

Similar to macroalgae, benthic microalgae arealso important primary producers on illuminatedshallow-water sediments. On sediments where thereare no macroscopic primary producers, they are theonly benthic primary producers, forming the basefor benthic food webs. Benthic microalgae are mostwell studied on tidal mud- and sandflats, but arealso important in subtidal habitats, particularly inmicrotidal estuaries, where the water column oftenstays clear through most of the day because of thelack of strong tidally induced turbidity. In large deepestuaries, such as Chesapeake Bay, a high percentageof the sea floor is within the photic zone, enablingprimary production to occur over large areas.

8.4.2 Hard-Bottom: Rocky Intertidal,Shallow Subtidal

Rocky intertidal and shallow subtidal zones world-wide are dominated by macroalgae, microalgae, andsessile invertebrates. While common along opencoasts, some rocky areas exist in sheltered estuarinesystems such as fjords and sounds. The rockyintertidal zone is characterized by environmentalextremes (temperature, salinity, desiccation, nutrientsupply), yet there are also strong biotic interactionsthat combine to produce striking patterns of zonationalong elevational gradients. Both macroalgae andmicroalgae play important roles as in situ producers,forming the base of local food webs.

Macroalgae in rocky intertidal habitats arehighly diverse and abundant, especially in temperate

regions. Virtually every functional form of macroal-gae can be found in hard-bottomed habitats, fromdelicate branching genera such as Plocamium to largeand fleshy reds and browns such as Mastocarpus(Turkish Towel) and Egregia (Feather Boa Kelp).Many classical studies have identified the importanceof top–down forces in controlling the structure ofrocky intertidal communities (e.g., Connell, 1972;Paine, 1974). More recent work has begun to focuson bottom–up processes as well as the relationshipbetween biodiversity and ecosystem functions suchas productivity and nutrient retention (e.g., Wormand Lotze, 2006; Bruno et al., 2008). Although rockyintertidal and shallow subtidal systems in tropicalregions are far less studied, there is some evidence tosuggest that macroalgal communities in some areas,such as the Pacific coast of Panama, are controlledby the same ecological processes as temperatesystems (Lubchenco et al., 1984). In polar regions, theextreme and variable light climate and continuousnear-freezing temperatures impose constraints onmacroalgal production and depth distribution, asareas are typically ice covered for all but two monthsof the year. Despite these harsh conditions, crustosecoralline macroalgae can be found down to 50 mdepth in Arctic estuaries where the light level isonly 0.004% of surface irradiance (Rysgaard et al.,2001). Large brown algae in the genera Laminariaand Fucus are often the community dominants in the2–20-m-depth region attached to rocks, stones, andeven gravel in protected areas (Witman and Dayton,2001; Krause-Jensen et al., 2007). Physical disturbanceby ice scouring often limits the distribution atshallow depths, and light limitation and possibly alsodisturbance from walrus feeding activities sets thelower limit of distribution in Arctic waters (Borumet al., 2002; Krause-Jensen et al., 2007).

Although macroalgae are the most prominentvegetation of rocky shores, there is also another lessevident, but ecologically important algal community,the microscopic epilithic (growing on rock) commu-nity. Rocky surfaces are covered by a biofilm compris-ing microalgae, cyanobacteria, and newly germinatedstages of macroalgae. This often slippery biofilm alsoincludes bacteria, protozoans, and meiofauna. In theupper intertidal, cyanobacteria give the rock surface adark, almost black color. Typical cyanobacterial gen-era are Rivularia and Calothrix. However, the blackcolor can also be due to salt-tolerant lichens, such asVerrucaria maura. Epilithic diatoms often include lifeforms that are stalked and form colonies (for example,the genera Gomphonema, Fragilaria). The biofilm is animportant food source for limpets and periwinkles


and also influences the settlement of invertebrate lar-vae. In addition to a top–down control by grazers,the algae in the intertidal biofilm are controlled byphysical stress caused by high insolation (Thompsonet al., 2004).

8.4.3 Coral Reefs

Coral reefs are productive, diverse, and economicallyimportant ecosystems that dominate hard-bottomedhabitats in low nutrient tropical and subtropicalwaters. They proliferate in open nearshore habi-tats and in sheltered lagoons along tropical andsubtropical coasts. On pristine coral reefs, fleshymacroalgae are rarely spatially dominant (Littler andLittler, 1984); rather, tropical reefs in low nutrientwaters are dominated by crustose coralline and turf-forming algae. These algae form the base of benthicfood chains, contribute to biodiversity, and stabi-lize reef framework. Crustose coralline algae playan important role in reef accretion, cementation, andstabilization (Littler et al., 1995). Algal turfs, compris-ing filamentous algae and cropped bases of largerforms, are ubiquitous throughout tropical reefs andare characterized by high rates of primary produc-tivity. An exception to dominance by corallines andturfs on pristine reefs can occur when mechanismsexist which limit the efficacy of herbivores. Physicalor chemical defenses produced by macroalgae such asDictyota and Sargassum, and spatial refuges from her-bivory such as surrounding sand planes or the basesof branching corals, can support fleshy macroalgae(Hay, 1984; Smith et al., 2010). Human impacts onreefs such as overfishing of herbivorous fishes (Jack-son et al., 2001; Hughes et al., 2003) and increasednutrient supplies (Smith et al., 1981; Lapointe et al.,2005) may also produce dominance by macroalgae.

8.5 SPATIAL PATTERNS OFBIOMASS AND PRODUCTIVITY8.5.1 Broad GeographicScale—Latitudinal Differences

Benthic macroalgae are found in subtidal and inter-tidal estuarine habitats from tropical to polar regions.Some macroalgal species have broad geographic dis-tributions, indicating their ability to acclimate toclimatic variations in temperature and irradiance.For example, the foliose Laminaria saccharina occurs inrocky subtidal habitats from Spain to North Green-land (Luning, 1990), and coralline algae inhabit watersthroughout tropical and polar regions (Steneck, 1986).

Mesoscale differences in annual rates of productivityare related predictably to temperature and irradi-ance levels. Rates of productivity can be as high as2500 g C/m2/year (Valiela, 1995), and highest annualrates are in tropical communities where growth andtemperature conditions are favorable throughout theyear. In regions where water column productivity islow, as in the tropics and some polar regions, benthicmacroalgal production can exceed pelagic produc-tion on an areal basis (Duarte and Cebrian, 1996;Krause-Jensen et al., 2007).

Benthic microalgae are found on every surfacethat is reached by light. While benthic microalgaeexist in all climatic zones, their temporal and depthdistribution varies with latitudinal light conditionsand the transparency of the water column. The rangeof annual benthic microalgal primary productionvaries from 5 to over 3000 g C/m2/year, but mostvalues are within the range 20–500 g C/m2/year(Cahoon, 1999), and the highest values are from trop-ical regions. Areal values of both daily net primaryproduction (NPP) and chlorophyll a (a rough measureof microalgal biomass) are often similar in magnitudeto those for phytoplankton in shallow, clear water ofthe coastal regions. In shallow (1–3 m) estuaries, ben-thic microalgae can account for up to 70% of the totalprimary production (Underwood and Kromkamp,1999; Baird et al., 2004), and in areas that lack macro-scopic primary producers, they constitute the onlyautochthonous benthic source of primary production.Even in temperate seagrass meadows, the contribu-tion of benthic microalgae can be 20–25% of thetotal benthic primary production (Asmus and Asmus,1985). In tropical and subtropical seagrass-vegetatedsediments, the biomass of benthic microalgae can beas high as that in adjacent unvegetated sediments,even though the seagrass canopy reduces light avail-ability at the sediment surface (Miyajima et al., 2001).

8.5.2 Depth Distribution

Benthic macroalgae contain accessory pigments thatallow capture of different wavelengths of light andefficient utilization of changing light quantity andquality with depth in the water column (Fig. 8.2). Redalgae contain accessory pigments such as phycoery-thrin that absorb green and blue-green wavelengthsthat penetrate deep in clear coastal waters. Crus-tose coralline red algae are the deepest living marinemacroalgae, and have been found at depths of 268 min the clear, tropical waters of the Bahamas whereirradiances were less than 0.001% of the surface irra-diance (Luning and Dring, 1979). These macroalgaeare characterized by slow growth rates. Light atten-uation with depth, and the changing quality of light

Spatial Patterns of Biomass and Productivity | 209

The quantity and quality of photosyntheticallyactive radiation (visible light) changes with depth.Blue and green light penetrates deepest.

All algae havechlorophyll a (white linein top graph)

Green algae also havechlorophyll b and aregenerally limited to shallowor very clear water

Brown algae have auxiliarypigm ents such asfucoxanthins that enablethem to proliferate atinterm ediate depths

Red algae can survive at thedeepest depths as auxiliarypigm ents such asphycoerythrin absorb theblue and green light

Although auxiliary pigments enable algae to extend their ranges deeper, this does not mean that theyare limited to those depths! Red algae, for example, can live intertidally as well as deep. In addition,other factors such as grazing, wave energy, and disturbance control algal depth zonation.

Artwork by Kendal Fong

FIGURE 8.2 Different divisions of algae have adapted to the varied light regimes that occur along depth gradients in estuaries.

limits the potential depth distribution of macroal-gae, although disturbance and grazing losses alsoinfluence the actual depth distribution (Fig. 8.2). Theminimum light requirements for thick macroalgae(∼0.12% of surface irradiance) and thin macroalgae(<0.005%) are substantially less than those for mostseagrasses (∼10–25%, see Chapter 5), and as a resulttheir depth penetration is much greater than that forthe vascular plants (Fig. 8.3).

As for macroalgae, the depth at which benthicmicroalgal primary production is important dependson the transparency of the water body. In clearwaters, benthic microalgal NPP can be substantial atdepths >20 m and can be sustained at a light level of5–10 µmol photons/m2/s (Cahoon, 1999). At a site inNE Greenland, the maximum depth limit for benthicmicroalgae matched the 50 m depth limit for crustosecoralline macroalgae, where light was 0.004% of the

Light

Maximum depth of survival

Maximum light requirements:

Seagrass ~11%, thick macroalgae ~0.12%, thin macroalgae ~0.003%

FIGURE 8.3 Comparison of minimum light requirements between macroalgae and seagrass. Depth limits are set by lightattenuation in the water column.


surface irradiance during the open-water season(Rysgaard et al., 2001).

8.5.3 Energy Regime

Flow velocities around macroalgal thalli can havepositive effects on rates of nutrient uptake and photo-synthesis by reducing the thickness of the boundarylayer and increasing the exchange of gases and solutesacross the thallus surface (Hurd, 2000; Hepburn et al.,2007). In dense macroalgal communities, flow veloc-ity is reduced due to the drag imposed by the thalliand this increases particle deposition and decreasesparticle resuspension (Gaylord et al., 2007; Morrowand Carpenter, 2008). Reduced flow rates can alsoinfluence macroalgal growth. For example, Stew-art et al. (2009) showed that in dense beds of thegiant kelp Macrocystis pyrifera, fronds on the seawardedge of the bed had faster elongation rates, largerblades, and greater carbon and nitrogen accumula-tion than interior fronds that were exposed to lowerflows. Flow velocities also decrease with depth inthe subtidal, and maximum velocities typically occurat the subtidal–intertidal fringe (Denny et al., 1985).Biomechanical models for high energy systems (upto 15 m/s) can be used to calculate velocities thatcause macroalgal thalli to break and thus predictsurvival against hydrodynamic forces (Denny, 1995).The two most important factors determining breakforces for macroalgae are substrate type and thallussize (Malm et al., 2003). In low energy systems, waterspeeds as low as 0.22 m/s can cause both breakageand ‘‘pruning’’ (thallus fragments left for regrowth)for attached algae with delicate thalli such as Ulva(Kennison, 2008). The macroalgal form can vary inresponse to flow regimes, with exposed areas havingalgae with flatter, narrower fronds to reduce dragand protected areas having wider, undulate fronds toincrease turbulent flow and decrease boundary layereffects. This can reflect both morphological plasticityand genetic differentiation (Hurd et al., 1997; Rober-son and Coyer, 2004).

The largest accumulations of macroalgae arefound in poorly flushed systems, such as shelteredembayments and estuaries, with elevated nutrientconcentrations where bloom-forming species occur(e.g., Ulva sp., Chaetomorpha sp., Gracilaria sp,Polysiphonia sp.) (Viaroli et al., 1996; Pihl et al., 1999).Advective transport of macroalgae, both betweenhabitats within an estuary (i.e., subtidal to intertidal)and from the estuary to the coastal ocean, can beimportant in terms of nutrient exchange. Macroalgalmaterial moves either as bedload or as floating matsat the water surface, depending on their specificgravity (which is influenced by photosynthesis

rates and invertebrates that colonize mat-formingmacroalgae). Unattached, living macroalgae move atcurrent velocities as low as 2 cm/s (Flindt et al., 2004),and these current velocities are common in estuarieswhere both winds and tides affect current speeds atthe sediment surface (Lawson et al., 2007; Kennison,2008). Macroalgae also settle 1000 to 5000 times fasterthan phytoplankton, and hence if transported out ofestuaries usually settle on the ocean floor rather thanbeing returned on the flood tide (Flindt et al., 2004).Few studies include mass transport of nutrientsbound in plant material and as a result nutrientretention in estuaries can be overestimated.

Generally, benthic microalgal production ishigher in fine sediments than in sandy sedimentsexposed to wave action (Underwood and Kromkamp,1999). The explanation for this finding is that finesediments, with high organic matter concentrationand rapid bacterial mineralization, contain morenutrients in the pore water than sandy sedimentswith less accumulation of organic matter. Moreover,the biomass of benthic microalgae (measured aschloropyll a content of the sediment) in the upperfew millimeters of muddy sediments can be muchhigher than in sandy sediments. But the NPP canoccasionally be as high, or even higher, in sandythan in muddy sediments. One reason is the higheravailability of light, because of a thicker photic zone,so that photosynthesis can occur deeper in sandysediments than in muddy sediments. In addition,advective flushing can reduce nutrient limitation ininundated permeable sands (Billerbeck et al., 2007).In high energy environments, such as tidal sand flats,a large part of the benthic microalgal community canbe resuspended during the tidal cycle, contributingto pelagic production. Up to half of the food resourceof filter feeders can consist of resuspended benthicmicroalgae (de Jonge and Beusekom, 1992). Theturnover of benthic microalgal biomass on sandytidal flats is typically higher than that on muddy flats(Middelburg et al., 2000).

8.6 TEMPORAL PATTERNS OFBIOMASS AND PRODUCTIVITY8.6.1 Diel Cycle

The diel cycle of benthic microalgal primary produc-tion is well described, and generally differs betweentidal and subtidal sediments (Fig. 8.4; Miles andSundback, 2000). On muddy tidal flats, there are largevariations in the light climate during the day because

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FIGURE 8.4 Diel pattern of microphytobenthic primary production (bars) on a shallow-water subtidal sandy site (Kattegat,microtidal west coast of Sweden) and an intertidal muddy site (Tagus estuary, Portugal). Measurements were made by the14C technique with subsequent 2-h incubations during three full days. Filled circles show irradiance measured at sedimentsurface. Because of high turbidity, no light penetrated to the sediment surface during high tide in the Tagus estuary. Source:Redrawn from Miles and Sundback (2000).

of tide-induced turbidity, and photosynthesis occursonly when the sediment is immersed during daylight.This pattern is strengthened by the endogenous (i.e.,controlled by ‘‘internal clocks’’) vertical migrationrhythm of particularly motile diatoms. The algaestart to migrate down 30–60 min before the tidereturns (Kromkamp and Forster, 2006) and emergeagain to the surface for the low tide period (Fig. 8.1b).High resolution techniques, such as low tempera-ture scanning electron microscopy and single-cellpulse–amplitude–modulation (PAM) chlorophyllfluorescence, have shown that the algal compositionat the sediment surface changes during the photope-riod (Underwood et al., 2005). This vertical migrationcan be explained as a way of taking advantageof the favorable light conditions during low tideand avoiding resuspension by the tidal waves. Amore stable habitat with higher concentrations ofnutrients also provides more favorable conditionsfor cell growth and division deeper in the sedimentcompared to the sediment surface (Saburova andPolikarpov, 2003). On sandy tidal flats, the watercolumn may stay clear during high tide, and primaryproduction can continue when the sediment issubmerged. In subtidal habitats and on microtidalcoasts, the light climate is often not affected by tidalturbidity, and benthic photosynthesis can proceed

throughout the daylight period (Fig. 8.4), showingthe highest production at midday. Benthic diatomsalso migrate daily in subtidal conditions so that theyemerge before sunrise and submerge in the evening(Longphuirt et al., 2006).

8.6.2 Seasonal Cycle

Seasonality in benthic algal growth is highest in polarregions and decreases toward lower latitudes. Forperennial macroalgae in polar regions, shade adap-tation is one way of dealing with the dark wintermonths and the ice cover 10 months of the year. Lam-inarians that dominate these regions have inherentlyslow growth rates, storage of carbon reserves duringthe summer period of high productivity, a long lifespan, and a high resistance to grazing (Luning, 1990).Macroalgae need to maintain low respiration to min-imize carbon losses during the long winter months,high photosynthetic efficiency at low light when icestill covers the water surface, and the ability to max-imize continuous light in the summer. Laminariansincrease their blade surface area to increase light cap-ture and produce new thin blades before the breakup of ice cover using stored reserves in old overwin-tering thalli and are poised for rapid growth as soonas the ice-free period begins (Chapman and Lind-ley, 1980; Dunton, 1985). In temperate soft-bottom


systems, macroalgae may be present year-round,and different species have different thermal toler-ances and optimum temperatures for photosynthesis,respiration, and growth, so species composition canchange with increasing temperature. In general, therespiration rate increases more rapidly with risingtemperature than photosynthesis rate, leading to adecrease in the photosynthesis:respiration ratio (P/R).

Ephemeral macroalgae go through boom andbust cycles in many regions, with the mid-growingseason population crashing due to high temperaturesand self-shading. In some areas such as southernCalifornia, floating blooms can occur during anyseason, with the magnitude and frequency relatedto land use in watersheds and patterns of nutrientinput (Kamer et al., 2001; Boyle et al., 2004). Inter-tidal macroalgae on rocky shores, especially in highertidal zones, respond to interactions among monthlyand seasonal changes in the tidal amplitude, temper-ature, and light by changing biomass (Menge andBranch, 2001). Seasonality is much less pronouncedin tropical systems, although some exceptions occur.Some coral reef algae show marked seasonal variationin standing stock of carbon (Lirman and Biber, 2000).On Panamanian reefs, algal productivity and biomassaccumulation is much higher during the upwellingseason (Smith, 2005), suggesting that algal commu-nities are regulated by nutrients in the absence ofupwelling.

Seasonal variability in thallus photosynthesis ishigher for ephemeral macroalgae than for perennialgenera such as Cladophora and Ulva that grow fastand store little nutrient reserves (Sand-Jensen et al.,2007). Respiration rates typically vary systematicallyover the year, and increase as temperature and irra-diance levels increase. For temperate species, thisleads to higher minimum light requirements duringsummer than winter for photosynthesis to balancerespiration. While there are significant changes inthe actual production as light and temperatures varywith seasons, the maximum potential production (atsaturating light) varies less (Middelboe et al., 2006).This is in part due to changes in species compositionand abundance that favor species that have optimalperformance at different times of the year.

Long-term studies on seasonality of benthicmicroalgae are rare. One of the longest seasonalstudies (12 years, 14 stations) on benthic microalgalbiomass and production is from a tidal flat on thecoast of the Netherlands (Cadee and Hegeman,1977). This study shows that, in temperate areas, thebiomass peaks during the warm season. Occasionaldips in benthic chlorophyll a during summer areexplained by strong grazing pressure, particularly by

mud snails (such as Hydrobia ulvae). This seasonal pat-tern agrees with patterns found in shallow subtidaland microtidal areas in temperate estuaries, althoughwell-developed diatom mats have also been found onthe sediment surface under sea ice. Such proliferationof benthic diatoms under ice can be explained bythe presence of shade-tolerant species, good nutrientavailability, and low grazing pressure. In tropicalareas, seasonal variations in benthic microalgalabundance can be influenced by the monsoon, suchthat abundance is lowest during the monsoon andhighest during the postmonsoon period (Mitbavkarand Anil, 2006). In polar regions, the length of theproductive season for benthic primary productionis only about 80–90 days. During this period, thedaily microbenthic primary production (172–387 mgC/m2/day) at depths ≤20 m has been found toexceed that of phytoplankton (Glud et al., 2002).

8.7 METHODS FORDETERMINING PRODUCTIVITYFor macroalgae, various methods are used to estimateproduction, based either on short-term estimates ofcarbon assimilation/oxygen production or on longer-term growth estimates.

1. Growth Measurements Frond-marking is acommon technique used to estimate growth rates oflarge, attached macroalgae such as kelps. The fronds,or blades, are marked with holes at the junctionbetween the stipe and the blade where the growthzone is located. The holes are displaced upward asthe blade grows and the distance between the holeand the stipe/blade junction represents new growth(Krause-Jensen et al., 2007). This is similar to the leaf-marking technique that is commonly used to measureseagrass growth. Rates of elongation are then con-verted to production as mass (gram dry weight, gdw)or carbon using conversion rates. For unattached matsor rafts of macroalgae with diffuse growth (growththroughout the thallus), the biomass can be measureddirectly as wet weight. Algae are collected from aknown area of benthos or volume of water, cleanedof mud and fauna, and, if desired and possible, sep-arated into species. Techniques to assure a consistentwet weight are varied, but include blotting the thallidry or spinning in a salad spinner for a consistenttime and rate. The change in the average biomassover time estimates productivity.

2. Photosynthesis Measurements Measurementsof net or gross production as gas (O2 or CO2) exchange

Methods for Determining Productivity | 213

provide shorter-term estimates of production, andthese can be scaled spatially and temporally based onavailability of incident irradiance. Changes in oxygenor dissolved inorganic carbon (DIC) can be mea-sured on individual thalli in light or dark bottlesor chambers to estimate the NPP and respiration.Photosynthesis–irradiance (P–I) curves can be con-structed for each species to derive data on maximumphotosynthetic rate (Pmax), efficiency of light uti-lization (a), respiration (R), and the saturation andcompensation irradiances (Is and Ic) (Chapter 4).These parameters can be related to light availabil-ity at specific water depths using an equation (e.g.,P = Pmax[1 − exp(aI/Pmax)] + R; Platt et al., 1980) andscaled to areal rates of production.

Since macroalgae can grow in dense accumula-tions, models are used to account for self-shadingwithin the macroalgal communities (Brush andNixon, 2003; McGlathery et al., 2001). These modelsscale production in macroalgal mats based onincident irradiance reaching the canopy, knownpatterns of light attenuation with depth in macroal-gal mats, and P–I relationships for individualthalli. This approach is similar to terrestrial canopymodels. Sand-Jensen et al. (2007) have modified thisapproach further to consider variations in thalluslight absorbance, canopy structure, and density. Themodel has been tested for single-species communitiesof the sheetlike Ulva lactuca and the leathery Fucusserratus and for mixed-species communities. Aninteresting result of the model is the stabilizingeffect of species richness, whereby multiple speciescomplement each other in absorbing light.

The PAM chlorophyll a fluorescence technique isalso used to determine relative measures of photosyn-thetic activity of algal species. These measurementstypically provide a snapshot (seconds–minutes) ofphotosynthetic capacity to acclimate to light con-ditions. However, they do not easily translate intoquantitative measures of photosynthesis in terms ofoxygen production or carbon fixation. The PAM tech-nique can be used in situ and measures the activityof photosystem II, giving an estimate of the electrontransport rate (ETR). Although there is a fairly goodlinearity between ETR, oxygen production, and 14Cincorporation, this relationship can become nonlinearat high irradiances. For a review on this technique seeKromkamp and Forster, (2006).

For benthic microalgae, the best methods for pri-mary production measurements are those that do notdisturb the natural physical, chemical, and biologicalmicrogradients in the sediment. There are four prin-cipal methods that are used for primary production

measurements in sediments. All these techniqueshave their limitations, and primary production ratesdetermined by the different methods can be slightlydifferent because they measure different aspects ofphotosynthesis.

1. Sediment–Water O2 or CO2 Exchange Oxygenflux is measured as changes in the concentrationof oxygen in well-mixed overlying water in benthicchambers or sediment cores. The advantage of thismethod is that the measurements integrate over asediment area and that measurements both in thelight and dark give three ecologically relevant rates:net primary production (NPP), community respira-tion (CR), and gross primary production (GPP). Fieldmeasurements of benthic primary production on tidalflats during immersion are possible by measuringCO2 fluxes in benthic chambers (Migne et al., 2004).Disadvantages are that cores and chambers do notreplicate natural hydrodynamic and light conditionsand may underestimate the flux.

2. Uptake of Radioactively Labeled Carbon(14C-Bicarbonate) This is a suitable technique fortracking the fate of carbon in food webs. In sandysediments, 14C can be percolated a few millimetersinto the photic zone of the sediment (Jonsson, 1991).In muddy sediments, percolation does not usuallywork, and the technique relies on diffusion of thelabel into the sediments, which results in underes-timation of primary production. Slurry incubationsdisrupt the microgradients in the sediment, butare suitable in experiments where the maximumpotential primary production is used as a variable.The stable isotope 13C also can be used for trackingcarbon through the food webs (Middelburg et al.,2000).

3. Oxygen Microsensors (with a Tip of Only aFew Microns) and Planar Optodes These are usedfor high-resolution nondestructive measurements ofoxygen microgradients in the sediment, from whichprimary production can be calculated by modeling(Fig. 8.5). The dark–light shift microelectrode tech-nique can also be used to measure oxygen production(Revsbech et al., 1981). The classic oxygen microsen-sor is the oxygen electrode with a guard cathode(Revsbech, 1989), but there are also oxygen optodesthat are based on fiber optics (Glud, 2006). The useof microsensors has contributed greatly to our under-standing of the temporal and spatial variations amongthe processes operating in the top few millimeters ofthe sediment. Planar optodes make it possible to geta two-dimensional picture of the O2 distribution anddynamics at a given area over many days (Fig. 8.5;Glud, 2006). Such measurements have provided new


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insights into oxygen dynamics around rhizopheres,faunal structures, structures in permeable sands, andwithin phototrophic communities.

4. PAM Chlorophyll a Fluorescence The fluores-cence technique can be used to estimate photosyn-thesis in the sediment microalgal community andalso to measure photosynthetic activity of individ-ual cells using a modified fluorescence microscope(Underwood et al., 2005)

Finally, for all types of benthic producers, thereis a new in situ method based on the eddy correlationflux technique that is commonly used to measureoxygen exchange across the land–air interface interrestrial and intertidal ecosystems. This techniquehas been adapted to subtidal conditions and has theadvantage that it measures community metabolismunder natural hydrodynamic and light conditions,can capture short-term (minutes) variation in produc-tion/respiration, and integrates over a much largerarea (>100 m2) than conventional techniques (<1 m2)(Berg et al., 2003, 2007).

8.8 FACTORS REGULATINGPRODUCTIVITY ANDCOMMUNITY COMPOSITIONThe mechanisms that control the net production ofbenthic algae in estuarine ecosystems are the sameas those for other primary producers: geographiclimits for growth are set by temperature and light.Within the geographical limits, biomass accumula-tion is controlled by many interacting biotic andabiotic factors including light quantity and qual-ity, nutrient availability, water motion, temperature,intra- and interspecific competition, grazing, andphysical disturbance. Here we discuss light, nutri-ents, and grazing; additional factors are included inother sections.

8.8.1 Light

Similar to all primary producers, benthic macro-and microalgae use visible light in the 400–700 nm

Factors Regulating Productivity and Community Composition | 215

spectrum, which is termed photosynthetically activeradiation (PAR). Accessory pigments in benthic algaeallow certain groups to capture wavelengths thatwould otherwise be inaccessible by chlorophyll aalone (Fig. 8.2). Light is attenuated exponentiallywith depth in the water column following theBeer–Lambert law, Iz = I0eKdz, where Iz is the irradi-ance at depth z, I0 is the surface irradiance, and Kdzis the attenuation coefficient for diffuse downwellingirradiance. This is described in detail in Chapter4. The surface irradiance reaching the benthos ata given depth is influenced by properties of thewater that affect the attenuation coefficient, includingsuspended sediment, organic (e.g., phytoplankton)and detrital particles, and colored organic matter(CDOM).

Light is attenuated rapidly within dense macroal-gal communities. For the bloom-forming speciesCladophora prolifera and Chaeomorpha linum, 90% ofthe available irradiance hitting the surface of themat can be absorbed in the top few centimeters(Krause-Jensen et al., 1996). The extent of thislight attenuation will depend on the thallus form(canopy structure) and density of the algae, theabsorbance of the algae, and species composition.Complementarity of light use between differentalgal species in mixed-species communities oftenmeans that the total community production is higherfor a given irradiance level than for single-speciescommunities (Middelboe and Binzer, 2004). Benthicmacroalgae can acclimate rapidly (within minutes) tochanging light conditions. This can be an adaptationfor optimizing production in a short growing season(Borum et al., 2002) or to a variable light climatedue to short-term changes in incident irradiance(e.g., cloud cover) or water column light attenuation(e.g., wind/wave induced sediment resuspension).A general adaptation to reduced light levels is anincrease in pigment content and light utilizationefficiency. This results in reduced compensationand saturation irradiances (Ic, Is) for photosynthesis.These characteristics allow macroalgae to more effec-tively photosynthesize at low light levels. However,the production and maintenance of higher pigmentcontent and enzyme activities increase respiratorycosts in low light plants. At high irradiance levels,pigment concentrations are typically lower, compen-sation and saturation irradiances are higher, andmaximum photosynthesis is high. Photoinhibitionmay occur at high irradiances or under high UVstress, and the damage to the photosystem thatcauses this inhibition is not necessarily reversible(Chapter 4).

Benthic microalgae also function in a wide rangeof light climates and are able to adapt to widelyfluctuating light conditions. Diatoms can optimizetheir photosynthetic apparatus efficiently to currentlight conditions (within minutes) (Glud et al., 2002).Moreover, as epipelic life forms are able to migratevertically in the sediment, they can position them-selves in favorable light conditions. In this way, phys-iological photoinhibition is avoided at high ambientlight levels. Because of back-scattering effects, thelight intensity at the sediment surface can be up to200% higher than the ambient light above the sedi-ment (Kuhl et al., 1994). While the photic zone in thewater column is generally measured in meters, thephotic zone in shallow-water sediments is measuredin micro- and millimeters. Fiber-optic microsensorsenable high resolution measurements of the lightquantity and quality in microbial mats and surfacesediments (Kuhl et al., 1994). Light penetrates deepestin sandy sediments (∼3 mm), while in fine sedimentsthe photic zone is less than 1 mm. The light climatein the sediment also differs from that in the watercolumn in that red light penetrates deepest in sedi-ments. The vertical change in the light quantity andspectrum often results in stratified microbial matsconsisting of layers of organisms with different opti-mal light requirements (e.g., a sequence of diatomson the top, followed by cyanobacteria, and then byphotosynthetic purple sulphur bacteria, which preferanaerobic conditions). Live microalgae can be foundfar below the photic zone in the sediment. Episammicdiatoms on sand grains can be mixed down to 10 cmdepth in wave-exposed sediments. They survive longperiods (weeks, months) of darkness, and rapidlyresume photosynthesis when transported up to thephotic zone by mixing of the sediment.

8.8.2 Nutrients

8.8.2.1 SourcesBenthic algae obtain nutrients from both the sed-

iments and the water column and the source ofnutrients are from both external (allochthonous) andrecycled (autochthonous) sources. Sources of ‘‘new’’or allochthonous nutrients include terrestrial inputsvia rivers from coastal watersheds, nitrogen fixation,groundwater, atmospheric deposition, and upwelling(Nixon, 1995; Smith et al., 1996; Whitall and Paerl,2001). With the possible exception of upwelling andN-fixation, all of these sources are rapidly increas-ing as a result of anthropogenic alterations of globalnutrient cycles (for a review, see Vitousek et al., 1997).Autochthonous sources of nutrients include recyclingfrom other biota and regeneration from the sedimentsduring decomposition.


8.8.2.2 Uptake and StorageThe relationship between the nutrient concen-

tration in the water and the rate at which nutrientsare taken up by benthic macro- and microalgaecan be described by a hyperbolic function. TheMichaelis–Menten equation for enzyme uptakekinetics is often used to describe this function, andthis is also described in detail for phytoplankton inChapter 4. The Michaelis–Menten equation describesuptake as follows: V = Vmax

∗[S/(K + S)], where Vis the uptake rate at a given substrate (nutrient)concentration, S is the substrate concentration, Kis the half-saturation concentration—where uptakeis equal to 1/2 of the maximum uptake rate, andVmax is the maximum uptake rate at high substrateconcentration. From a biological perspective, thereare two important components of this relationship:(i) nutrient uptake rates become saturated as nutrientconcentration increases and (ii) the initial slope ofthe curve at low concentrations provides a usefulindex of an alga’s affinity for nutrients at lowlevels. This latter characteristic may be important indetermining the competitive abilities of algae whennutrients are in critically low supply. The Vmax ratevaries depending on the nutrient status of the plant.Algae that have lower nitrogen contents in morenitrogen-limiting environments would be expectedto have higher maximum nutrient uptake rates.

For macroalgae, uptake rates are higher forthin-structured sheetlike or filamentous thalli that

have a high surface area to volume ratio thanfor more coarsely branched species (Fig. 8.6, Wal-lentinus, 1984). In addition, some nitrogen-starvedephemeral macroalgae have the capacity for veryrapid (‘‘surge’’) uptake during the first minutes ofexposure to nutrients, which results in a three-phasepattern of nutrient uptake as a function of externalsupply (Pedersen, 1994). The capacity for surgeuptake is assumed to be advantageous for ephemeralalgae subject to short-term nutrient pulses thatmight result from animal excretion or temporarilyhigh mineralization rates. For macroalgae, thereare two primary ways to measure nutrient uptake:(i) the ‘‘multiple flask’’ method, where differentsubstrate concentrations are added to individualflasks containing macroalgae, the disappearanceof substrate is measured over a short (15-min)incubation, and then the data are pooled to obtainan uptake versus concentration curve; and (ii) the‘‘perturbation’’ method, where thalli are exposed toa high concentration of substrate and a time series ofsubstrate concentration is measured (Pedersen, 1994).

Both macro- and microalgae can store nutrients,and their capacity to do this varies depending ontheir inherent growth rates and the frequency andmagnitude of nutrient pulses. The general patternthat emerges is that fast-growing ephemeral macroal-gae such as Ulva and Chaetomorpha store little reservescompared to slow-growing perennial species such asFucus, which has reserves that can support growth forlonger periods of time. This influences the duration

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Factors Regulating Productivity and Community Composition | 217

of nutrient limitation that often occurs in temperateregions in response to a seasonal (summer) deple-tion of nutrients. For example, Pedersen and Borum(1996) showed that while different algal species, fromphytoplankton to slow-growing perennial macroal-gae, had similar storage reserves (mg N/gdw), thestorage capacity, that is, the ability to support growthin the absence of an external nutrient supply, variedfrom less than 1 day for phytoplankton to greaterthan 15 days for perennial macroalgae (Fig. 8.7). Onshorter time scales (hours–days), macroalgae haverapid, but transient, responses to variability in Navailability, with uptake rates influenced by chang-ing tissue N pools (McGlathery et al., 1996). Also, thecoupling of C metabolism (photosynthesis and stor-age) and N metabolism over the short term impliesthat algal growth rate acts as a feedback regulatorto maintain balanced C-N metabolism, except underextreme conditions of high irradiance and low N sup-ply. Such self-regulation may be especially beneficial

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to algae growing in estuarine environments that arecharacterized by high spatial and temporal variabilityin nutrient and light availability (McGlathery andPedersen, 1999).

8.8.2.3 Limitation of GrowthIn most temperate and polar estuaries, nitrogen

is considered to be the primary limiting nutrientfor growth, in part due to high rates of denitrifi-cation relative to nitrogen fixation. For macroalgaein tropical/subtropical systems dominated by car-bonate sediments, phosphorus often limits growth,largely due to the binding of phosphorus by thecarbonate sands. There are exceptions to this general-ization that are related to the ratio of N:P in externalloading, variations in the relative rates of nitrogen fix-ation and denitrification, and the adsorption capacityof carbonate sediments in different systems. Largedata sets on C:N:P ratios of marine plants indicatethat macrophytes (macroalgae and seagrasses) havedifferent characteristic atomic ratios of tissue nutri-ents than phytoplankton. Atkinson and Smith (1983)examined marine plants and found a ratio of 550:30:1for benthic marine plants, and Duarte (1992) showedthat the ratio for 46 macroalgal species was 800:49:1.These ratios compare to the ‘‘Redfield Ratio’’ of phy-toplankton of 106:16:1 (Chapter 4), and suggest thatmacroalgae have a higher nitrogen demand. As withphytoplankton, these ratios are often used to infernutrient availability and possible nutrient (N vs P)limitation.

Increases in nutrient supplies that relieve nutrientlimitation in subtidal soft-sediment habitats result inenhanced macroalgal production and potentially inthe loss of seagrasses, which tend to dominate underlow nutrient conditions (see Chapter 5 and Duarte,1995; Valiela et al., 1997; McGlathery et al., 2007).In salt marshes, water column nutrients sequesteredby understory macroalgae are retained within thesalt marsh community, and become available to sup-port vascular plant growth when macroalgae senesce(Boyer and Fong, 2005). Transitions from macroalgaeto toxic cyanobacterial mats occur in estuaries on theWest Coast of the United States (Armitage and Fong,2004), perhaps due to higher tidal amplitudes, lowerresidence times, and broad areas of intertidal mud-flats (large areas of suitable habitat). Nutrient-drivencommunity shifts also occur in rocky intertidal areas(Worm et al., 2002; Worm and Lotze, 2006). In thesestudies, experimental nutrient enrichment increasedmacroalgal abundance, and grazing by consumersmoderated that response. However, macroalgae inareas with low ambient nutrients responded to enrich-ment with increased thallus complexity and diversity,


while macroalgae in more enriched areas respondedwith decreases in diversity due to a shift in dominanceto opportunists.

For coral reefs, there is considerable debate aboutwhether algae are limited by nutrients. Effects ofexperimental nutrient additions have varied from noeffects (Delgado et al., 1996; Larkum and Koop, 1997;Koop et al., 2001) to orders of magnitude differencesin effects on photosynthesis, growth, and biomassaccumulation (Lapointe and O’Connell, 1989). Inter-pretation of experimental results is limited, in part,by the difficulty of relating results of laboratory ormicrocosm studies to natural growth in the highenergy, high flow environments with variable nutri-ent supply typical of coral reefs (Fong et al., 2006),and by the related methodological challenge of effec-tively conducting in situ experiments in these sameenvironments (reviewed in McCook, 1999).

It was once generally assumed that benthicmicroalgae are not likely to be limited by nutrientsin the same manner as phototrophic organisms inthe water column. This is often the case for fine sed-iments, but in sandy sediments, benthic microalgaecan be nutrient limited (Nilsson et al., 1991). For shortperiods, however, nutrient limitation can also occurin fine, cohesive sediments during, for example, tidalemersion (Thornton et al., 1999). Studies on nutrientfluxes in well-sorted permeable sandy sedimentsexposed to wave action have, on the other hand,partly changed our view on the nutrient limitation insandy sediments. In permeable sediments, nutrientavailability can be enhanced by efficient advectivetransport, resulting in high microbenthic primaryproduction (Billerbeck et al., 2007).

8.8.3 Grazing

Preferential feeding by herbivores can influence theabundance and species composition of macroalgae.Many studies show an association between highnutrient content of primary producers and high con-sumption rates; however, other factors such as her-bivore abundance, per capita grazing rates of thedominant herbivores, and feeding preferences alsoplay important roles in determining patterns of her-bivory (Cebrian, 1999, 2002).

Herbivory has been shown to control algalbiomass accumulation with community-level effects.For example, grazers such as amphipods and gas-tropods can control the abundance of algal epiphyteson seagrasses and hard substrates, and can mediatethe negative shading effects of epiphytes in responseto nutrient loading (Williams and Ruckelshaus, 1993;Hillebrand et al., 2000). Likewise, grazers can medi-ate the impact of macroalgal blooms in eutrophic

environments (Worm et al., 2000). On coral reefs,at low to intermediate nutrient supplies, herbivorescan control macroalgal abundance and maintain thecompetitive dominance of slower-growing commu-nity types (Hughes et al., 2003; Pandolfi et al., 2003).Rapid growth with nutrient enrichment allows algaeto escape control by herbivores and also biomassto accumulate, which ultimately leads to a phaseshift. Chemical and structural defenses also providea refuge from control by herbivores, allowing algalbiomass to accumulate even in heavily grazed areas.In soft-sediment communities, enhanced algal growthfrom high nutrient loading can saturate the grazingpotential and decrease per capita consumption rates;grazer abundance can be impacted negatively bythe change in physicochemical conditions (i.e., lowoxygen, high sulfide and NH4

+) that result from thedecomposition of algal blooms (Hauxwell et al., 1998).

Microbenthic primary production can enterthe food web through several pathways, includingthrough grazers, detritus, or dissolved organiccarbon (DOC). Field studies show that a largefraction of benthic microalgal biomass can passthrough macrograzers (>1 mm), particularly mudsnails (Hydrobia) (Asmus and Asmus, 1985; Andresenand Kristensen, 2002). In addition, some microphy-tobenthic production can pass through the ‘‘smallfood chain’’ consisting of microfauna (unicellularfauna such as ciliates) and meiofauna (<100 µm)(Fenchel, 1968; Kuipers et al., 1981; Pinckney et al.,2003). Meiofauna have been estimated to occasionallygraze up to 100% or more of the benthic microalgalstanding stock, although benthic primary productionis generally sufficient to supply food resources formeiofaunal grazers (Pinckney et al., 2003).

8.9 ENERGY FLOWThe amount of energy sequestered in primaryproducers and the proportion flowing through algal-dominated benthic estuarine communities variesamong soft sediment, coral reef, and rocky intertidaland subtidal ecosystems (Fig. 8.8). In all systems, theamount of energy that is fixed into algal biomass andmade available to higher trophic levels is dependenton resources, usually light and nutrients. Overall,systems more closely associated with terrestrialenvironments, and those that experience restrictedwater exchange, such as those composed of softsediments, are assumed to be subject to and affectedthe most by increasing external nutrient supplies.

Energy Flow | 219

Resources

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(a) Soft sediments

(b) Coral reefs

(c) Rocky intertidal and subtidal

FIGURE 8.8 Energy flow diagrams for different macroalgal communities. The size of the arrow represents the magnitude offlow in the different pathways.

8.9.1 Recycling of Nutrients

Across estuarine systems, recycling of nutrients fromsediments and biota is most likely greatest in softsediment and coral reefs and least in rocky inter-tidal and subtidal systems. In soft-sediment estuariesand lagoons, fluxes of nutrients regenerated fromsediments are an important source of recycled nutri-ents (McGlathery et al., 1997; Fong and Zedler, 2000;Tyler et al., 2003). In some seasons, fluxes meet up to100% of macroalgal nutrient demand (Sundback et al.,2003). Interception of nutrients by macroalgae mayreduce supplies to other producer groups and changethe path and rate of carbon flow. Macroalgal com-munities may also be sustained by nutrient releasefrom senescent or self-shaded thalli, or by recyclingof nutrients from nearby vascular plant communitiessuch as seagrass beds (for a review, see McGlathery

et al., 2007). In coral reef ecosystems, recycling fromsediments is only likely to be significant in enrichedsystems (Stimpson and Larned, 2000). Other recycledsources in coral reefs include flocculent material set-tling on the surfaces of algal thalli (Schaffelke, 1999)and animals that release nitrogenous waste prod-ucts (Williams and Carpenter, 1988). Release of wasteproducts from closely associated animals is also arecycled source of nutrients in intertidal and subtidalsystems (Hurd et al., 1994; Bracken, 2004).

8.9.2 Carbon Storage

The capacity of ecosystems to store energy, repre-sented by the amount of carbon in the biomass ofproducers and consumers, varies across estuarineecosystems. An example is the tremendous differ-ence in producer biomass between coral reef algae(0.03–0.6 kg wet weight/m2 based on a wet:dry


weight ratio of 10:1, Foster, 1987) and rocky subtidalreefs (3.5 kg wet weight/m2, Manley and Dastoor,1987). Although both are highly productive in termsof gross primary productivity, they occupy differentends of a spectrum in terms of biomass accumulationand therefore carbon storage. In general, opportunis-tic species with simple thallus forms such as those thatdominate coral reef turfs have low levels of biomass;therefore, they can store little carbon despite hav-ing relatively rapid growth rates. The low biomassis due to short life spans, susceptibility to removaland export by physical disturbance, and high ratesof grazing by herbivores. In contrast, more com-plex macroalgae that dominate rocky subtidal andintertidal areas often have high standing stocks ofcarbon. This is due to the longevity of individualthalli, investment in structure to withstand physicaldisturbances, and lower rates of carbon transfer toherbivores due to protection by chemical and phys-ical defenses. One exception to this generalizationis opportunistic macroalgae in shallow soft-sedimentestuaries that go through periods of boom and bustand cycle carbon quickly.

8.9.3 Herbivory

The amount of energy that is transferred frommacroalgae through consumption can vary by ordersof magnitude across estuary types. On a globalscale, direct consumption by grazers was estimatedto be 33.6% of the net carbon fixed by macroalgae,demonstrating their general importance as the baseof food webs in coastal ecosystems (Duarte andCebrian, 1996). Herbivory on coral reefs is extremelyhigh, with large herbivorous fishes and invertebratesacting as ‘‘lawn mowers’’ that keep algal standingstocks very low and carbon transfer very high (fora review see McCook, 1999; Jackson et al., 2001).In rocky subtidal habitats, grazing is important inmaintaining diversity, but cannot always overcomethe effects of increased resources (Worm and Lotze,2006). Within soft-sediment systems, rates of primaryconsumption can vary greatly (Fong et al., 1997;Giannotti and McGlathery, 2001), and consumptionof benthic microalgae can be very important (Asmusand Asmus, 1985; Armitage and Fong, 2004).

Benthic microalgal production forms the basis forthe benthic food webs in sediments where macro-scopic primary producers are lacking. The main path-way of this fixed carbon into the food web is generallyconsidered to be through macrofaunal and meiofau-nal grazers (Duarte and Cebrian, 1996), although thedetrital pathway is also important. The microbial film(epilithon) on rocky surfaces is an important compo-nent in the cycling of carbon, particularly on exposed

and moderately exposed shores with large numbers oflimpets and other grazers (Hawkins and Jones, 1992).

8.9.4 Detrital Pathway

Death and subsequent decomposition of macroal-gal detritus results in the release and recycling ofstored carbon. Processing of carbon through detritalpathways comprises about a third of macroalgal netprimary productivity globally (Duarte and Cebrian,1996). However, like grazing, the relative importanceof recycling varies across habitats. For example, highenergy rocky areas recycle much less carbon fromdetritus within the system compared to lagoons, whilethe estimates for recycling within coral reef algae arevery high (Duarte and Cebrian, 1996). When algaedecompose, they release organic carbon to the waterand, in soft sediments systems, to the sediments (fora review see McGlathery et al., 2007). The detritalpathway is also important for benthic microalgaeproduction (Admiraal, 1984). As much as 70% of theNPP by benthic microalgae on a tidal flat was foundto enter the food web as detritus (particulate organiccarbon, POC), and was further transferred to bacteriaand detritus-feeding fauna (Baird et al., 2004).

8.9.5 Dissolved Organic Carbon

Substantial DOC also ‘‘leaks’’ from healthy macroal-gal thalli (Tyler et al., 2003; Fong et al., 2003).Some organic compounds in the water can betaken up directly by consumers and may alterfood webs toward heterotrophic bacteria pathways(Valiela et al., 1997). A large portion (>50%) ofthe photosynthetic product of benthic microalgaecan also be released as DOC, particularly underlow nutrient conditions. This DOC enters foodwebs rapidly through bacteria (Middelburg et al.,2000), forming the benthic equivalent of the pelagialmicrobial loop. About 40% to 75% of the carbonfixed by motile benthic diatoms can be released ascolloidal organic matter or EPS (Goto et al., 1999;Smith and Underwood, 2000) and rapidly transferredto sediment bacteria.

8.9.6 Export of Carbon

The rate of carbon exported from benthic estuarinecommunities varies tremendously across ecosystemtypes and is a function of standing stock, watermotion, and algal morphology. Duarte and Cebrian(1996) have calculated that a global average of 43.5%of macroalgal NPP is exported; however, the rangeis perhaps the more important metric, varying fromapproximately 0–85% across macroalgal-dominatedhabitats. Rocky subtidal systems export a far larger

Feedbacks and Interactions | 221

amount of carbon than coral reefs despite vigorouswave action in both systems due to the larger stand-ing stock. In contrast, pristine soft sediment lagoonalsystems export less carbon than rocky systems asthere is both less physical disturbance and lowerwater exchange to detach and remove biomass. Thus,seagrasses in lagoons represent a large and relativelystable reservoir of carbon. In contrast, in eutrophicsystems there is often accumulation of large float-ing algal rafts, resulting in faster turnover and morerapid export of carbon to the ocean (Flindt et al.,1997; Salomonsen et al., 1999). In sediments exposedto strong tidal or wave action, benthic microalgae areeasily resuspended together with sediment particlesand hence can be transported away (Admiraal, 1984).A large study in the Ems-Dollart Estuary (North Seacoast) showed that, on an annual basis, 14–25% of themicrophytobenthic carbon was found in the watercolumn as a result of resuspension (de Jonge andBeusekom, 1995).

8.10 FEEDBACKSAND INTERACTIONS8.10.1 Feedbacks on BiogeochemicalCycling in Soft-Sediment Estuaries

Both macro- and microalgal mats have a large impacton the biogeochemical cycling in shallow-water habi-tats. This effect can be both direct, through nutri-ent assimilation, retention, and release, and indi-rect through oxygen production and consumption,affecting mineralization and other redox-sensitiveprocesses. Despite large differences in biomass, thequantitative role of macroalgal and microalgal matson biogeochemical processes (for example, nitrogenassimilation) can be similar, making the turnovertime of algae-bound nutrients a key factor in nutrientretention in shallow systems (McGlathery et al., 2004).Nutrients that are assimilated by benthic algae are,for the most part, only temporarily retained withinindividual algal thalli on a time scale of days tomonths. Tissue turnover times vary for the differentautotrophs, with seagrasses having a longer retentiontime (weeks–months) than bloom-forming macroal-gae (days–weeks) and microalgae (days). This sug-gests that nutrients will be recycled faster in systemsdominated by microalgae and ephemeral macroalgaethan in those dominated by perennial macrophytes(Duarte, 1995).

Both types of benthic algal mats stronglyinfluence the degree of benthic–pelagic coupling byreducing the flux of remineralized nutrients from the

sediment pore water to the overlying water column(Sundback et al., 1991; Fong and Zedler, 2000; Ander-son et al., 2003; Tyler et al., 2003; see also Section8.10.5). Benthic algae can outcompete phytoplanktonfor nutrients if the major nutrient supply is internalflux from the sediments. Therefore, in shallow coastalsystems, short-lived phytoplankton blooms oftencoincide with low benthic algal biomass (Sfriso et al.,1992; Valiela et al., 1992; McGlathery et al., 2001). Theinfluence of benthic microalgae on sediment–waternutrient fluxes is often observed as lower fluxes—orno flux at all—out of the sediment in light whencompared with that in the dark (Sundback et al., 1991;Sundback and McGlathery, 2005). When sedimentnutrient sources are insufficient to meet the growthdemand of benthic microalgae, there is a downwardflux from the water to the sediment, such that thesediment functions as a temporary nutrient sinkinstead of a nutrient source. This applies particu-larly to autotrophic sediments (oxygen productionexceeds oxygen consumption, Engelsen et al., 2008).Also, dissolved organic nutrients, such as dissolvednitrogen (DON), are influenced by both benthicmicro- and macroalgae (Tyler et al., 2003; Veuger andMiddelburg, 2007).

Benthic algal mats influence the vertical profilesof oxygen and this affects biogeochemical cycling.The presence of dense macroalgal mats can move thelocation of the oxic–anoxic interface up from the sed-iments into the mat since only the upper few centime-ters of the mat are in the photic zone where oxygenis produced by photosynthesis (Krause-Jensen et al.,1996; Astill and Lavery, 2001). Below the photic zone,decomposing macroalgae release nutrients that candiffuse upward to support production. Unattachedmacroalgal mats tend to be patchy and unstable, butoxygen and nutrient gradients develop quickly, in aslittle as 24 h, suggesting that this filtering functionoccurs even in dynamic environments (Astill andLavery, 2001). Overall, sediment nutrient cycling isenhanced by the presence of macroalgae, presumablydue to the input of organic matter and faster decom-position (Trimmer et al., 2000; Tyler et al., 2003). Inthe surface layer of the sediment, dynamic oxygengradients created by benthic microalgal activity alsocontrol the rate and vertical position of the sequenceof redox-sensitive processes in the sediment, suchas nitrification, denitrification, sulfate, iron and man-ganese reduction, and methane production.

Benthic micro- and macroalgae have an importantinfluence on rates of denitrification and nitrification.Rates tend to be low in sediments underlying macroal-gal mats, likely due to algal competition with bacteriafor NH4

+ and NO3−. In addition, high free sulfide


concentrations in organic-rich sediments underlyingmacroalgal accumulations may inhibit nitrification(Trimmer et al., 2000; Dalsgaard, 2003). In densemacroalgal mats, the zone of denitrification may bemoved up from the sediments into the oxic–anoxicinterface of the mat (Krause-Jensen et al., 1999). Thecombined use of oxygen and nitrogen microsensorshas shown that benthic microalgae can both reduceand enhance denitrification. During photosynthesis,the oxygenated sediment layer gets deeper, and ittakes longer for the NO3

− to diffuse from the watercolumn to the denitrification zone of the sediment,reducing the rate of denitrification. Under low nitro-gen conditions, benthic microalgae will also competewith nitrifying bacteria for NH4

+, reducing the avail-ability of substrate (NO3

−) for the denitrifiers. Suchan effect by benthic microalgae can still occur downto a water depth of 15 m (Sundback et al., 2004). Whenambient N concentrations are high, oxygen produc-tion will instead stimulate nitrification (an aerobicprocess), and thereby also stimulate nitrification-coupled denitrification (Risgaard-Petersen, 2003). Thealternative pathway of bacterial nitrogen removal,anaerobic ammonium oxidation (anammox), is neg-atively affected by the presence of active benthicmicroalgae (Risgaard-Petersen et al., 2004).

8.10.2 Feedbacks on SedimentStabilization

Macroalgal mats may either stabilize or destabilizesediments, depending on algal abundance. Densemacroalgal mats stabilize sediments by decreasingshear flow at the sediment surface (Escartın andAubrey, 1995) and thus sediment suspension (Sfrisoand Marcomini, 1997; Romano et al., 2003). Thickmacroalgal mats (equivalent to 3.5 to 6.2 kg wetwt/m2) displace velocities vertically and can deflect90% of the flow over the mat, with only 10% ofthe flow traveling through the mat (Escartın andAubrey, 1995). However, macroalgae also exist at lowdensities and in patchy distributions that are oftendependent on available substratum for attachmentor on advection of drift algae (Thomsen et al., 2006)and may act to destabilize sediments. At low densi-ties, flow causes macroalgae to move and scour thesediment, increasing sediment suspension relative tobare sediments. This sediment destabilization is akinto the well-documented phenomenon of saltating orabrading particles increasing erosion in cohesive sed-iments (e.g., Houser and Nickling, 2001; Thompsonand Amos, 2002, 2004). In cohesive beds, the criti-cal stress required to initiate erosion is often greaterthan the stress required to maintain the sediment insuspension. Macroalgae that scrape the bed while

moving across it can dislodge particles and increasesediment suspension/erosion.

The influence of benthic microbial mats on sur-face sediment stability is well studied (e.g., Paterson,1989; de Brouwer et al., 2006). The mechanism behindthis stabilizing effect is the production and extru-sion of EPS by diatoms through the raphe duringtheir gliding movements. Its composition can be com-plex and varies between species, but mainly consistsof carbohydrates, proteins, and sulfate groups. EPSbind sediment particles together so that the shearstress needed for erosion of sediment is increased, andtherefore the sediment is less easily eroded and resus-pended. Besides gluing sediment particles together,EPS also have physiological and ecological implica-tions. On tidal flats, there are large diel changes inenvironmental variables (light, temperature, salinity,water content, oxygen, and erosive forces). By secret-ing EPS, the diatoms become embedded in a cohesivematrix that can create more stabile conditions. Thissediment stabilization is a seasonal phenomenon atleast in temperate systems, and the deposited mate-rial may be resuspended at times of the year when themicroalgae are less productive (Widdows et al., 2004).

8.10.3 Effects on Faunal Biomass,Diversity, and Abundance

Macroalgae can have positive and negative effects onassociated organisms. On the positive side, they canprovide a food source through direct assimilationor through detritus-based food chains, as well asa protective refuge from predators (Norkko andBonsdorff, 1996). The complex structure of somemacroalgal species, such as Gracilaria vermiculophylla,could potentially create a predation refuge forcommercially valuable blue crab and fish recruitsas well as shrimps and amphipods in both thesubtidal and lower intertidal zones of estuaries (Hayet al., 1990; Thomsen et al., 2009). Macroalgae alsomay provide an important link between estuarinehabitats (subtidal to intertidal, sand flats to seagrassbeds), as associated organisms are transferred withadvecting macroalgae between habitats (Holmquist,1994; Thomsen et al., 2009).

The negative effects of dense macroalgae onbenthic fauna include harmful exudates that are toxicto some organisms, low dissolved oxygen within andunder dense macroalgal mats (Hull, 1987; Isakssonand Pihl, 1992), and high dissolved NH4

+ concen-trations that also can be toxic (Hauxwell et al., 1998).These negative effects have been associated withobserved reductions in abundance of various macro-fauna, including bivalves, gastropods, amphipods,and fish, as well as increases in certain polychaetes,

Environmental Impacts | 223

oligochaetes, and amphipods (Norkko and Bonsdorff,1996; Raffaelli, 2000; Wennhage and Pihl, 2007).

Both macro- and microalgal mats can cause neg-ative upward cascades in estuarine food webs. Forexample, microalgal mats subjected to high nutri-ent loads shifted to dominance by cyanobacteria andpurple sulfur bacteria and increased the mortalityof the dominant herbivore, the mudsnail Cerithidiacalifornica, threefold over mats subjected to lowernutrients that were dominated by diatoms (Armitageand Fong, 2004). Changes in benthic fauna associ-ated with macroalgal blooms may cause resident andmigratory shorebirds to change foraging behavior.For example, sandpipers spend more time probing intheir search for food when they are foraging on top ofmacroalgal mats, but more time repeatedly peckingwhen mats are absent (Green, 2010). As infauna area major food source for birds and other secondaryconsumers, macroalgal impacts that reduce this linkin the food chain may impair this vital ecosystemfunction. There is also growing evidence that indirectpositive effects in the form of ‘‘facilitation’’ cascadesmediated by habitat created or modified by macroal-gal species can enhance biodiversity and organismalabundancs (Thomsen et al., 2010).

8.10.4 Facilitation by Fauna

Macroalgae in soft-bottom environments can be facili-tated by fauna, such as tube-dwelling polycheates andbivalves, that provide hard substrate for settlementand growth. For example, the tube-cap forming poly-chaete, Diopatra cuprea, facilitates macroalgal assem-blages in shallow lagoons. These organisms createand maintain attachment sites by incorporating algalfragments into tube caps, thus increasing algal resi-dence time on mudflats compared to unattached algae(Thomsen et al., 2005). This association both increasespopulation stability and resilience by providing astable substrate that retains algae against hydrody-namic forces such as tidal flushing and storm surge,and by providing new fragments to populate newareas or repopulate areas after a storm disturbance.Oyster reefs and mussel and clam beds likewise pro-vide substrate for algal attachment and increase bothbiomass and diversity relative to nearby bare sedi-ments (McCormick-Ray, 2005). These biotic substratesalso enhance algal growth by local fertilization effects.Grazers such as the California Horn Snail can facilitatethe development of macroalgal mats by consumingmicroalgal competitors and releasing nutrients foruptake by macroalgae (Fong et al., 1997). Also, oncoral reefs, Carpenter and Williams (1993) showedthat urchin grazing facilitated algal turf production byreducing self-shading within the dense algal turf com-munity. Invertebrate grazers that remove microalgal

films that sometimes form on macroalgal thalli, but donot damage the macroalgae, may facilitate macroalgalgrowth by enhancing nutrient and gas exchange.

8.10.5 Competition between BenthicAlgal Primary Producers

Competition between benthic and pelagic algae wasmentioned briefly in Section 8.10.1. Here we discussthe interplay between mats of benthic microalgae andloose mats of opportunistic macroalgae in shallowwater in more detail (Fig. 8.9).

Benthic micro- and macroalgae interact, directlyand indirectly, through their impact on light, oxy-gen, and nutrient conditions. The type and strengthof the interactions change with the growth phase,physiological state, the spatial location of the matsin relation to each other, and the type of the waterbody as it relates to tidal amplitude. Shading by densemacroalgal mats generally decreases benthic microal-gal production. However, shade-adapted microphy-tobenthic communities that remain active—and eventhrive—below macroalgal mats are also present, pro-vided that at least some light penetrates to the sedi-ment surface (Sundback and McGlathery, 2005). Anexample of such a shade-adapted species is the largesigmoid diatom Gyrosigma balticum. Benthic microal-gae, particularly diatoms, are in fact often resistantto short-term (days, few weeks) hypoxia and anoxiaand promote recovery of sediment systems by rapidlyreoxygenating the sediment surface after hypoxic andanoxic events (Larson and Sundback, 2008).

When nutrient concentrations in the water col-umn are low, primary producer groups compete fornutrients. In such a situation, the importance of sedi-ments as a source of remineralized nutrients increases.At the same time, an active benthic microalgal matwill decrease the availability of sediment nutrients,limiting the growth of loose macroalgal mats, as wellas phytoplankton. In Figure 8.9, two conceptual mod-els are shown: one where the macroalgal mat (MA)exists close to the sediment surface (Fig. 8.9 a, b)and the other where the macroalgal mat is floatingat the water surface (Fig. 8.9 c, d). The coupling alsodepends on the thickness of the macroalgal mat andthe time of the day (day/night, tidal cycle).

8.11 ENVIRONMENTAL IMPACTS8.11.1 Eutrophication

As estuarine systems become increasingly eutro-phied and macroalgal blooms occur, the decomposingmacroalgal mats contribute significant amounts oforganic matter to the water and sediments (Trimmer


Thin MA mat (day):

• Algal mats coupled• Water/benthos decoupled

Night or thick MA mat (day):


Thin MA mat (day):

• Algal mats decoupled• Water/benthos decoupled

Night or thick MA mat (day):


Light

DCAA DCAAPO4 NH4+

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NO3− O2 O2

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MPB

MA

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All nutrients

All nutrients

Oxic sediment

Oxic sediment

Urea DFAA Urea DFAAAnoxic sediment

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(a) (b)

(c) (d)

FIGURE 8.9 Conceptual models of interactions between mats of benthic microalgae (microphytobenthos, MPB) and loosemacroalgae (MA). Upper panel (a and b): macroalgal mat lying close to the sediment surface, a situation common on tidalcoasts during low tide. Lower panel (c and d): macroalgal mat floating at the water surface, a typical situation in microtidalwaters. In (a), the two closely coupled mats intercept nutrient release from the sediment to the overlying water, whereas incase (b) nutrients are released from the anoxic sediment and the coupled mats to the overlying water. When the two algalmats are spatially separated (c and d), there is no nutrient exchange between the two mats or between the sediment andwater column. Instead, algal productivity is sustained by efficient recycling of nutrients within the mats themselves (c). Thisscenario applies particularly to autotrophic (often sandy) sediments in microtidal areas when nutrient levels in the overlyingwater column are low. At night, or when a thick floating macroalgal mat does not allow light to penetrate to the sedimentsurface (d), pore-water nutrients are released to the water column where they can be used by floating macroalgae. DFAArefers to dissolved free amino acids, and DCAA refers to dissolved combined amino acids. Source: Model drawings wereinspired by the model in Astill and Lavery (2001) and redrawn from Sundback and McGlathery (2005).

et al., 2000; Tyler et al., 2003; Nielsen et al., 2004). Thisdecomposing organic matter turns over relativelyquickly and is a positive feedback mechanismthat increases nutrient availability to sustain large

algal standing stocks. Other consequences of algalbloom formation in eutrophic estuaries includedecreases in fish/invertebrate abundance anddiversity, anoxia, and loss of seagrasses, corals,


and perennial algae (see 8.10). Eutrophication canlead to phase shifts from seagrass communities toalgal-dominated communities (Hauxwell et al., 2001;Valentine and Duffy, 2006), similar to what hasbeen observed in lakes and several other ecosystems(Scheffer et al., 2001; Scheffer and van Nes, 2004).It is essential to know whether these transitionsare reversible phase shifts or if they represent analternative state stabilized by negative feedbacks(Fig. 8.10).

Tropical estuaries with coral reefs may alsoundergo phase shifts from coral to algal domination(Knowlton, 2004), although the link to eutrophicationis less well established than for soft-sedimenthabitats. One classic study in Kaneohe Bay (Hawaii,USA) established that hard-bottomed communitiesshifted from coral to algae and back to coral againwith changes in nutrient loading. In this system,sewage outfalls into the Bay increased nutrientsand stimulated phytoplankton blooms. Lower lightpenetration stressed corals, shifting the competitiveadvantage to the macroalga Dictyospheria caver-nosa, the ‘‘green bubble algae’’ that was able tocreep over the substrate and replace coral. Aftersewage was diverted to an offshore outfall, waterclarity increased and coral gradually recolonizedand replaced the algae. However, while KaneoheBay is a clear example of a eutrophication-driventransition from coral- to algal-dominated tropicalreef communities, several other studies suggest thatco-occurring stressors, such as the loss of grazers,must be in play to shift these communities (Pandolfiet al., 2003).

The growth of benthic microalgae also mayrespond to increased nutrient load, particularlyin sandy sediments with lower concentrations ofpore-water nutrients than finer sediments (Nilssonet al., 1991). It appears that microphytobenthiccommunities are highly resilient to eutrophication-related disturbances and may play an important rolein the resilience of the sediment community after,for example, hypoxic and anoxic events (McGlatheryet al., 2007; Larson and Sundback, 2008). The negativeimpact of eutrophication on the benthic microalgalcommunity may be more gradual and slower thanfor benthic macroscopic primary producers such asseagrasses. Thus, a partial beneficial ‘‘buffering’’effect of benthic microalgae on shallow sedimentsystems may persist even in more heavily eutrophiedsystems. Microphytobenthic communities possess,owing to high diversity and functional redundancy,a certain degree of plasticity, increasing the overallresilience of shallow-water sediment systems afterpelagic bloom events. Benthic diatoms can survive

periods of only a few % of incident light (or evendarkness), and high sulfide levels, and can rapidlyresume photosynthesis when exposed to lightor after an anoxic event (Larson and Sundback,2008 and references therein). This scenario, withbenthic microalgae surviving despite deterioratingconditions, may apply particularly to areas wheremacroalgal bloom events last only a few months(Pihl et al., 1999; McGlathery et al., 2001; Dalsgaard,2003), leaving the rest of the year open to benthicmicroalgal primary production. In warm, eutrophicmicrotidal systems with long-lasting macroalgalblooms, benthic microalgae can be outcompeted byshading and also by dystrophic events when themacroalgal blooms eventually collapse (Viaroli et al.,1996).

8.11.2 Invasions

A recent review by Williams and Smith (2007) iden-tified a total of 277 introduced macroalgal speciesin marine waters worldwide. The primary vectorsfor invasion are boat traffic and aquaculture. Mostreports are from temperate regions; there is a generallack of information on introduced species fromtropical waters, especially coral reef habitats (Colesand Eldredge, 2002). The taxonomic distribution ofinvasive species identified in the review included165 Rhodophytes, 66 Phaeophytes, 45 Chloro-phytes, and 1 Charophyte. Most successful invaderswere foliose and filamentous forms, followedby leathery and siphonous forms (Williams andSmith, 2007).

Several characteristics of successful invaders havebeen identified: rapid reproduction and the poten-tial for successful evolution in new habitats, rapidcolonization (including fragmentation as a sourceof new propagules), vegetative growth for popu-lation stability, rapid nutrient uptake and growthpotentials (‘‘weedy’’ species), antiherbivore defenses,and a wide environmental tolerance (Nyberg andWallentinus, 2005). Both physical disturbance (bykilling natives and opening space) and eutrophication(by relaxing resource competition) can make estuar-ine habitats more easily invaded. Some well-knowninvasions are those of Caulerpa taxifolia, Gracilariavermiculophylla, G. salicornia, Kappaphycus alvarezii,Hypnea musciformis, Sargassum muticum, and Codiumfragile (Fig. 8.11). In general, the community-leveleffects of invasive macroalgae are negative whenaccumulations are dense, and include shading ofnative algal species leading to decreases in abun-dance and diversity, decline in epifaunal and fishabundance, diversity and reproduction, loss of sea-grass, and increases in incidences of anoxia and


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Alternative stable states - shifts in responseto disturbance

The Nature of Community Collapse: Phase Shifts or Alternative Stable States?Macroalgae are taking over benthic estuarine communities worldwide. Catastrophiccollapses from long-livedseagrass and coral dominated ecosystems to opportunistic and shorter-lived macroalgae have focused researchon the nature of these shifts. One important question is whether these are simple and reversible phase shifts, orif they represent alternative stable stateswith stabilizing mechanisms that inhibit recovery to the initial state(Scheffer et al. 2001, Beisner et al. 2003, Didham and Watts 2005).

Management strategies differ if communities exist as alternative stablestates. Theory predicts there are only two ways to restore the initial, often moredesirable state.One is to reverse the environmental conditions far beyond the forward shift, to F2,often a very difficult and expensive option.The other is to cause a large disturbance that pushes the community beyond theunstable equilibrium (represented by the dotted lines), a strategy with unknown sideeffects.To distinguish phase shifts from alternative stable states scientists mustsearch for positive feedback mechanisms that stabilize each state that are strong enoughto buffer these states across a range of environmental conditions (betweenF1 and F2) andprovide resilience to small disturbances.

Phase shifts are rapid, catastrophic shifts from one dominantcommunity to another over a very short range of environmentalchange. Incremental changes in a environmental conditions causelittle change until a critical threshold is reached. Thus, the pasthistory of environmental change will not aid prediction of futurechange.

Communities that exist as alternative stable states also undergo rapid and catastrophicchanges. However, forward transitions occur at different points than backward transitionsresulting in a range of conditions (between F1 and F2) where either of two different states canoccur. Thus, there is limited ability to predict the community state based on the condition ofthe environment.

Why do we care?

Unstable equilibrium

FIGURE 8.10 The Nature of Community Collapse: Phase Shifts or Alternative Stable States?

hypoxia. There may be cases where introduced sea-weeds increase habitat structure and complexity onunvegetated mudflats, as is the case with G. vermicu-lophylla in some Virginia coastal lagoons, and have apositive effect on faunal abundances as long as algalpopulations stay below bloom proportions (Thomsenet al., 2009).

8.11.3 Climate Change

Climate change impacts on benthic algae include sea-level rise, increased temperature, increased CO2 inthe air and water, ocean acidification, and changes inweather patterns (Parmesan and Yohe, 2003). Risingtemperatures have been predicted to cause polewardshifts in geographic ranges of species and ultimatelyalter the composition of marine communities (for areview see Hawkins et al., 2008), including benthicprimary producers in estuaries. In temperate lati-tudes, warming may result in deepening thermoclines

and relaxation of cold upwelling, thus enabling warmwater species to more easily jump gaps in distribu-tion, especially along the western margins of majorcontinents. Continued temperature increases in trop-ical systems will likely result in further increases indominance of benthic algae as a result of coral bleach-ing and mortality (Hoegh-Guldberg, 1999). Changesin storm frequency may influence the distribution andabundance of benthic primary producers in estuariesby reducing or enhancing intertidal and shallow sub-tidal habitat via sedimentation, reducing water clarityand the depth of the photic zone, and increasingscouring (Zedler and West, 2008). For example, exper-imentally simulated scouring by sediments shiftedthe algal community from a diverse assemblage ofmacroalgae to more opportunistic forms (Vaselli et al.,2008) with high temporal variability (Bertocci et al.,2005) in rocky coastal habitats.

Some experimental evidence as well as stud-ies of aquaculture optimization techniques suggests


(a) (b)

(c) (d)

FIGURE 8.11 Many species of invasive red algae proliferate on Hawaiian coral reefs including (a) Acanthophora spicifera (b)Gracilaria salicornia, and (c) Kappaphycus alvarezii. (d) In some areas, such as the coast of Maui, blooms of Hypnea musciformisbecome so large that they detach, form floating rafts, and deposit on the beach. Source: Photographs by Jennifer Smith.

that increased CO2 concentrations and the resultantacidification of seawater may have strong effects onestuarine algae. Experiments with elevated CO2 andlowered pH have revealed strong negative effectson tropical crustose calcareous algae (Jokiel et al.,2008; Anthony et al., 2008), and also show that Por-phyra growth decreased with increased CO2, mostlikely due to increases in dark respiration rates (Israelet al., 1999).

There is also evidence that complex interactionsamong factors may be important. For example, whileincreased temperature and nutrients may increasealgal recruitment and growth up to some thresh-old, they should also increase the number of grazers,driving intertidal communities toward opportunisticspecies and away from dominance by fucoids (Lotzeand Worm, 2002). O’Connor (2009) found that warm-ing strengthens herbivore–algal interactions, shiftingimportant trophic pathways. Recent multifactorialexperiments show that certain stages in complex lifecycles may be more sensitive to interactions among

climate-related factors and may be important bottle-necks limiting the ability of algal dominants to surviveclimate change over the long term. For example, whileadult kelp sporophytes in polar regions are relativelyhardy to changes in temperature, UV light, salin-ity and their interactions, germination of zoosporesis much more sensitive (Fredersdorf et al., 2009).Aquaculture studies have identified an importantinteraction between rising CO2 and nutrients, withpositive CO2 effects on growth of Gracilaria beingaccelerated with pulsed nutrient supplies (Friedlan-der and Levy, 1995), suggesting that storms combinedwith rising CO2 will facilitate algal blooms in estu-aries. Other studies suggest that interactions amongclimate change factors may result in changes in habi-tats. In sheltered embayments of the North Sea, risingsea level and eutrophication combined to cause shiftsfrom Zostera to opportunistic green macroalgae (Reiseet al., 2008). Overall, it appears that interacting fac-tors associated with climate change will enhance algalblooms, and may shift communities to greater algaldominance.


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