LAND-WATER INTERFACES:
ATTACHED MICROORGANISMS,
LITTORAL ALGAE,
AND ZOOPLANKTON
I. Attached Microbes and Algae of Littoral
Regions
A. General Habitat Characteristics
B. Terminology and Zonation
C. General Distribution of Littoral Algae
D. General Structure of Periphyton
Communities
E. Growth-Regulating Resources
F. Growth-Regulating Mortality and
Losses
G. Community Analyses and Seasonal
Dynamics
II. Metabolic Interactions in the Littoral
Regions
A. Relationships between Algae and
Bacteria of Periphyton
Microbiota grow upon and attach to any surface
immersed or growing in water. The succession of mi­
croorganisms upon a surface is complex and involves
adsorption of organic substances to the surfaces and at­
tachment of microorganisms in sequence. Usually bac­
teria attach first followed by algae, cyanobacteria, and
protists. Extracellular mucilaginous materials, also re­
ferred to as exopolysaccharides or exopolymer secre­
tions (EPS), often occur as coatings around individual
microbial cells or projections from cells. Ultimately this
material forms a matrix inhabited by a variety of mi­
croorganisms, particularly bacteria, algae, protists, and
fungi (e.g., Fletcher and Marshall, 1982).
B. Effects of Light Availability
C. Attached Algae as a Source of
Phytoplankton
III. Productivity of Littoral Algae
A. Quantitative Evaluations
B. Biomass Measurements
C. Spatial and Temporal Variations
D. Production Rates of Attached
Algae versus Phytoplankton and
Macrophytes
E. Changing Littoral Productivity and
Eutrophication
IV. Periphyton among Aquatic
Ecosystems
V. Littoral Zooplankton Communities
VI. Summary
Excretion of exopolymer fibrils by bacteria is an
important initial phase of attachment of microbes to
surfaces (Fletcher and Floodgate, 1973; van Loosdrecht
et al, 1990; Brading et al, 1995). A substantial por­
tion of any attached aquatic microbial community will
be composed of nonliving, mucilaginous materials.
Most of this material is believed to be mucopolysaccha-
ride, although the exact composition and texture of it
varies with environmental conditions as well as the
nature and condition of the organisms that secrete it
(e.g., Sutherland, 1985; Hoagland et al, 1993).
Much excellent study has been directed to biofllms
attached to surfaces of technical devices (e.g., pipes,
577
578 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
Active Dormant-
Growth Senescent
FIGURE 19-1 Primary habitat and attached algal community components along a wetland-littoral gradient
of standing waters and backwater areas of river ecosystems. SWI = sediment-water interface; D = dark;
Lt = light. (Modified slightly from Wetzel, 1990a.)
ship hulls, and teeth) that convey or are immersed in
water (e.g., Characklis and Wilderer, 1989; Characklis
and Marshall, 1990). These studies correctly focus
largely on heterotrophic attached microorganisms, es­
pecially bacteria, because growth occurs on most of
these anthropogenic surfaces in darkness. In natural
ecosystems, however, algal photosynthesis is irrevoca­
bly coupled to heterotrophic attached microbial metab­
olism. As a result, mixed autotrophic-heterotrophic
assemblages form much more complex and metaboli-
cally dynamic communities than those that are only
heterotrophic.
I. ATTACHED MICROBES AND ALGAE
OF LITTORAL REGIONS
A. General Habitat Characteristics
Benthic algae and other autotrophic microbes, such
as the cyanobacteria, are generally associated with or
attached to substrata. These substrata are living or
dead, organic or inorganic, and in various combina­
tions. Because photosynthesis is the only significant
process for synthesis of organic matter among these
organisms, light is mandatory within both the macro-
habitats and the microhabitats of the communities in
sufficient quantities to allow net synthesis of ATP. The
land-water interface zone is a gradient that extends
from detrital masses in hydrosoils and pools of
wetlands through littoral zone regions of emergent,
floating-leaved, and submersed macrophyte communi­
ties to sediments extending into deeper waters well
Epipelic
Microflora
Microzone
of SWI
beyond the vascular macrophytes (littoriprofundal).
Available light shifts from abundant in wetland and
shallow nontree-canopied littoral areas to low and
highly variable seasonally in deeper areas as the densi­
ties of seston change in the overlying waters. Within
this zone of adequate light, substrata diversity is highly
variable but can be organized into general zones in
relation to potential substratum nutrient and other en­
vironmental characteristics (Fig. 19-1).
1. Emergent Plant Zones
These zones consist of saturated hydrosoils and
pools of upland wetlands and flood plains among
emergent macrophytes that are made up of largely of
standing and collapsed dead macrophytes and dense
aggregations of particulate detritus among the under-
story. Although many critical plant nutrients are re­
tained within living plant tissues and translocated to
rooting tissues at the end of growth periods of individ­
ual plant cohorts, soluble organic matter and organic
nutrients, particularly organic phosphorus, are released
from the highly productive emergent macrophytes dur­
ing and following active growth, senescence, and de­
composition (Chaps. 18 and 21). Many of these herba­
ceous perennials have more or less continuous leaf or
culm turnover of many cohorts per year in both north­
ern and southern regions. As a consequence, relatively
constant partial senescence of leaves and decomposi­
tion occur among macrophytes with release of cellular
organic matter and nutrients.
The high production of the emergent macrophytes
in excess of decomposition results in high detrital
organic matter accumulation at the sediment-water

interface. This loading, which contains relatively high
proportions of moderately recalcitrant structural
tissues from emergent plants, shrubs, and trees con­
tributes to high substrata surface area for microbial
colonization in relatively shallow water of high light
and temperatures. The high loading of organic matter
results in predominantly anaerobic conditions with
increased solubility of critical nutrients, particularly
P and N, in the interstitial waters near and at the
sediment-water interface (cf. Chaps. 12 and 13).
Much of the combined nitrogen as nitrate is commonly
denitrified by facultative anaerobic bacteria in such de-
trital-sediment masses and released to the atmosphere
as N 2 (Triska and Oremland, 1981; Bowden, 1987).
2. Submersed Plant Zones
As we have summarized in the Chap. 18, sub­
mersed macrophytes of lakes, ponds, rivers, and flood-
plain pools generally possess morphology of thin, finely
divided, and reticulated leaves. The resulting increased
surface area of leaves markedly enhances interceptions
of light and the exchange of gases with those of the wa­
ter. This greatly increased ratio of surface area to vol­
ume results in enormously increased substrata for colo­
nization by epiphytic algae, cyanobacteria, and other
microbes and protists. For example, the leaf surface
area available for colonization by epiphytic algae on
the submersed linear-leaved macrophyte Scirpus subter-
minalis averaged 24 m 2 of leaf area projecting upward
three-dimensionally above every square meter of bot­
tom in the moderately developed littoral zone of a lake
in southwestern Michigan (Burkholder and Wetzel,
1989). The extensive area of these macrophytic sur­
faces projects myriad diverse microhabitats with atten­
dant attached algal communities upward into littoral
environments. In this spatial habitat in the water col­
umn, relative abundance occurs of light, dissolved
gases from photosynthesis (0 2 ) and decomposition and
respiration (C0 2 ), and nutrients diffusing from the
high decomposition in interstitial waters of detritus and
sediments and imported from upland allochthonous
sources. Related to the very large diversity of micro-
habitats in this dynamic and highly productive region,
most (>80%) of freshwater species of algae and
cyanobacteria are attached, sessile forms (Round,
1981; Wetzel, 1999b).
3. Sediment Substrata
The benthic habitat in both standing and running
fresh waters can be a physically hostile yet nutritionally
advantageous environment. Epilithic and epipsammic
microbes, attached to rocks and sand grains, respec­
tively, are common in streams and wave-turbulent ar­
eas of lakes. Active water movements offer advantages
/. Attached Microbes and Algae of Littoral Regions 579
for nutrient and gas exchanges but also expose the
communities to molar action by particles such as sand
and potential burial by sediments with reduction or
removal of light (Meadows and Anderson, 1966; Moss
and Round, 1967). Most lakes and ponds are small
with modest fetch and wind-induced water movements.
Water turbulence also decreases rapidly with increasing
depth (cf. Chap. 7; also Imberger and Patterson, 1990),
and submersed macrophyte communities greatly atten­
uate flows in both lakes and streams (cf. Chap. 18). As
a result, even loosely aggregated organic-rich sediments
can serve as substrata for algae and cyanobacteria at­
tached to the surface of these sediments (epipelic) when
they receive adequate light. The unstable nature of such
sediments and frequently high rates of deposition from
settling seston increase the risk of epipelic algal burial
and light reduction. The high nutrient availability from
interstitial waters of sediments, however, is a distinct
advantage. Many epipelic algal species migrate, often
in rhythmic fashion, to compensate for shifting light at­
tenuation by sediment (cf. Round, 1981).
Algae growing adnate to unconsolidated, shifting
sediments are constantly in danger of being removed
from light, which is attenuated to zero in a few mil­
limeters.1 Whether epipelic algae supplement photosyn-
thetic growth by heterotrophic utilization of organic
substrates is unclear. Circumstantial evidence of the
high concentrations of organic substrates in the inter­
stitial waters of organic-rich sediments and many
epipelic algae growing under very low light conditions
is pervasive that facultative heterotrophy may occur
among some benthic algae (e.g., Gaines and Elbrΰchter,
1987; Tuchman, 1996). In spite of this physiological
potential, an important adaptation to the rigors of this
habitat is an ability to move vertically within the
sediments in response to light availability.
Persistent diurnal vertical migration rhythms have
been shown in epipelic diatoms, flagellates, and
cyanobacteria from flowing waters and shallow lakes
(Round and Happey, 1965; Round and Eaton, 1966).
Cell numbers on the sediment surface start to increase
before dawn and reach a maximum about midmorning.
Thereafter, surface cell numbers decrease and reach a
minimum before the onset of darkness. This rhythm
persists for a limited time in continuous darkness or
continuous light, although the synchrony is lost more
rapidly under continuous light conditions.
1
The attenuation of light by sediments is highly dependent upon the
type of sediment. Highly organic sediments attenuate light much
more rapidly than does sand. For example, Palmer and Round
(1965) found that radiation was reduced to about 1% of the
incident value under about 3 mm of organic-rich sediment. Similar
results were found by Wasmund and Kowalczewski (1982).
580 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
Studies of the diurnal rhythms of freshwater
epipelic algae have shown that the maxima of cell
emergence in the surface sediment layers and photosyn-
thetic capacity coincide, although the increase in pho­
tosynthesis preceded cell emergence (Brown et al.,
1972). The photosynthetic rhythm persisted at light
intensities well below saturation; minimum photosyn­
thetic values were found in midafternoon, after which
the rate increased again, a rise that preceded the
reemergence of cells. The maximum photosynthetic
rate occurred when maximum cell numbers were pre­
sent on the sediment surface.
4. Metaphyton
Loosely aggregated algae and cyanobacteria, the
metaphyton, in inundated water of wetlands and lit­
toral areas of many lakes, ponds, and floodplain areas
of rivers are neither strictly attached to substrata nor
truly suspended. Metaphyton communities originate
from fragmentation of dense epiphytic communities
that aggregate and become clumped and loosely at­
tached in littoral areas by wind-induced water move­
ments and then can form dense microbial accumula­
tions with intense internal nutrient recycling. The
productivity and collective metabolism of metaphyton
can be very high and radically alter the nutrient cycling
of littoral areas.
In contrast to the immense amount of study on the
systematics, physiology, and ecology of the phyto-
planktonic algae of aquatic systems, there is a dearth of
information on the algae attached to substrata or
loosely aggregated in the littoral regions of lakes or
shallow zones of streams and rivers. Although the taxa
of these largely sessile algae are somewhat better un­
derstood, information is sparse on their geographical
distribution, seasonal population dynamics, utilization
of microhabitats, responses to parameters of water
movement or water and substratum chemistry, or on
their interactions with other organisms.
The extreme heterogeneity in distribution of the al­
gae across an exceptionally variegated spectrum of mi­
crohabitats subjects attached organisms to much more
variable environmental physicochemical and biotic pa­
rameters than usually occur in the open water. Spatial
and temporal heterogeneity of phytoplankton in
pelagic habitats is minor in comparison to that of the
attached algae. Nonetheless, despite the numerous
problems associated with obtaining quantitative infor­
mation, indications are that the algal populations spe­
cialized to these habitats sustain high rates of produc­
tivity. Our poor understanding of the complex
interactions between the sessile flora and their sub­
strata, and the contributions of the attached microor­
ganisms to the total system productivity, represents a
major void in contemporary limnology that warrants
intensified study.
B. Terminology and Zonation
The limnological terminology applied to attached
algae is complex. These terms and the general zonation
of littoral algae have been introduced earlier (Chap. 8;
Fig 8-3, pp. 131-133).
C. General Distribution of Littoral Algae
Floristic surveys of the distribution of algae among
subcommunities of the littoral zone result in long lists
of species. Observed different associations reflect acute
heterogeneity in parameters of light, temperature, nu­
trient availability, water movement, substratum, graz­
ing pressure, and other factors. Detailed floristic analy­
ses indicate specific characteristics of dominant taxa
and designate the range of probable interactions among
species, thereby providing a foundation upon which
experimental approaches can be designed (Round,
1964a; Biggs, 1996; Stevenson, 1996a). The initial
evaluations often lead to recognition of algal associa­
tions in various habitats, thereby enabling quantitative
sampling and the separation of dominant and casual
species. These evaluations are difficult to perform,
especially among algae of the sediments, but have
been done in a number detailed analyses of littoral
communities.
The attached algae often dominate algal biomass in
small streams and shallow lakes. Probably > 9 0 % of
all algal species grow attached to a substratum; these
species include practically all of the pennate diatoms
and a majority of the Conjugales, Cyanophyta,
Euglenophyta, Xanthophyceae, and Chrysophaceae
(Round, 1964a; Biggs, 1996; Lowe, 1996).
Epilithic and epiphytic communities have many al­
gal species in common, but there is relatively little in­
terchange of species between those of the mud-living
epipelic habitat and the other substrata types. Epipelic
algae are largely motile; their motility is essential to en­
able them to move to the surface after any disturbance
of the sediments. Algal species adnate to sediments of
streams and rivers with moderate to fast flow are
almost exclusively motile.
Epipsammic algae, consisting largely of small di­
atoms and cyanobacteria attached more or less firmly
to crevices in the surface of sand grains and rock sur­
faces, exhibit an extremely variegated, heterogeneous
distribution (Fig. 19-2). These algae tend to be less
motile than epipelic algae, which usually grow on finer,
organic sediments (Round, 1965a; Meadows and
Anderson, 1966, 1968; Miller et al., 1987). In the

bare surface
deeply staining
patch
diatoms
bacteria
bacte blue green
algae
100/
FIGURE 19-2 Diagrammatic representation of typical localized
distribution of microorganisms and staining (carbol fuchsin) patches
of organic materials on the surface of a sand grain. (From Meadows,
P. S., and Anderson, J. G.: Micro-organisms attached to marine and
freshwater sand grains. Nature (London) 212:1059-1060, 1966.)
shallows of a temperate English lake, Moss and Round
(1967) found that both epipelic and epipsammic algae
showed marked population maxima during the spring.
The biomass of the epipsammic algae of the surface
5 cm of sediments was consistently greater than that of
the epipelic algae. Algal populations in interstitial wa­
ter of a sandy beach in a southern Michigan lake were
also large and exhibited a spring maximum (Davies,
1971). Percentage water content in sand sediments was
an important determinant of algal composition be­
tween the saturated zone of the water's edge and higher
sand beaches subject to periods of desiccation. Within
the sand, light is attenuated rapidly and is essentially
extinguished within half a centimeter. Yet viable epip­
sammic algae have been found attached to sand grains
as deep as 20 cm in sandy beach zones exposed to
heavy wave action. It is believed that wave action is ad­
equate to mix the sand grains and return attached algae
to a lighted zone sufficiently often to permit active, al­
though low, photosynthesis (Steele and Baird, 1968).
1. Attached Lichens of the Eulittoral
Lakes and streams with rocky shores and moder­
ately stable water levels may have an abundant and
diverse eulittoral crustose lichen flora. Largely studied
among waters of northern Europe, a characteristic
stratified zonation is commonly observed (Santesson,
1939; Hutchinson, 1975). Just above the lowest sum­
mer water level, grey-black Verrucaria spp. occur
epilithically, being submersed some 8 0 - 9 0 % of the
/. A ttached Microbes and Algae of Littoral Regions 581
year. Above this zone, some 2 0 - 3 0 cm above the low­
est water level, several lichens, dominated by blackish-
brown Staurothele, occur and are submersed well over
half of the year, mostly in winter., A higher association,
covered by water for 2 5 - 5 0 % of the year, is domi­
nated by light-brown or grey Lecanora spp. Above this
zone at about the highest water level, the lichens shift
to foliose species and associations. This distinct com­
munity demarcation, called the lichen line (Flechten
linie; Naumann, 1931), represents the most probable
highest water level in the immediate historic past.
Distribution of species within streams can be
delimited into four distinct zones in the British Isles
(James et al, 1977; Gilbert, 1996): (1) The fluvial sub­
mersed zone involves about 15, mainly pyrenocarpous,
species; (2) the fluvial mesic zone contains the richest
aquatic lichen flora, with about 20 species and approx­
imately 60% cover; (3) the fluvial xeric zone is lichen-
depauperate, being scoured by spates about once a
month; and (4) the lichen flora of the fluvial terrestrial
zone is influenced only by nutrient loading from the
stream water through the substrata. Along a stream
gradient, the lichen flora varies from species-rich head­
water flow with a cover of 80%» of exposed rock to
more erosive areas subjected to scour and substrata in­
stability where species diversity was low and cover of
bedrock was < 1 % .
Very little is known about the physiological char­
acteristics and constraints of these semiaquatic lichens,
although some of the ecophysiological factors that ac­
count for the delimited distribution of them have been
investigated (Ried, 1960a,b). Practically no species tol­
erates continuous submersion. A notable exception is
Hydrothyria venosa, a submersed species of the
Collemataceae characterized by hyphae that ramify
among the gelatinous matrix of single cells of the phy-
cobiont Nostoc (Russell, 1856). This rheobiont lichen
is rather commonly distributed on stones in relatively
quiescent mountain streams with its thallus often in
dense tufts to 10 cm or more in height. As in terrestrial
environments, semiaquatic and submersed lichens gen­
erally occupy harsh, austere habitats that are physically
stable and relatively free of nutrient enrichments and
siltation (Gilbert, 1996). Stable springheads of small
streams are common habitats in which interspecific
competition of lichens is low. It is suspected that
aquatic lichens usually possess slow growth rates and
contribute relatively small percentages to overall mater­
ial and energy fluxes of freshwater ecosystems.
The mineral content and pH of the water influence
the lichen flora as instanced by impoverishment of
communities on siliceous rocks on lakesides where
inflow streams are basic in composition. Lake and
stream lichens are also vulnerable to contamination by
582 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
inorganic fertilizers in runoff and seepage. Hypereu-
trophication encourages cyanobacteria and green algae
that can outcompete lichen communities. Long-term
studies of aquatic lichen communities are of value in
monitoring lowering or rising water levels that result
from human-induced alterations and diversions of wa­
ter (Seaward, 1996). River channel capacity can also be
determined by lichen zonation (Gregory, 1976).
D. General Structure of Periphyton Communities
Problems of exchange of nutrients, gases, and
metabolic products from within the periphyton com­
munities and the overlying water involve problems of
diffusion across the periphyton community boundaries
and the external medium. Slow diffusion into attached
microbial communities is particularly acute in relatively
thick communities, where high productivity is main­
tained by intensive internal recycling of nutrients, in­
cluding carbon, among mutualistic microbiota (Wetzel,
1992, 1993a). Abiotic adsorption of particulate and
dissolved organic compounds, as well as incorporation
of inorganic nutrients and metals into the mucilaginous
matrix, can provide a concentration mechanism (Lock,
1981, 1982; Lock et al, 1984; Roemer et al, 1984;
Beveridge and Graham, 1991; Freeman and Lock,
1995). Such concentration could enhance diffusion
within the community matrix to the organisms. This
mechanism likely not only stimulates the metabolism of
the community but in the case of certain cations, such
as calcium, magnesium, iron, and manganese, affect the
physical properties of the mucilage matrix, such as hy-
drophobicity (e.g., Freeman et al, 1995; Lemke et al.,
1995) and possibly texture. The extracellular matrix
can also provide sites for attachment for extracellular
enzymes, such as phosphatases and proteases, that are
critical in rendering nutrients and carbon available to
microorganisms (Wetzel, 1990a, 1991a).
Developing periphyton is three-dimensionally en­
meshed with hydrated glycocalyx and other mu-
copolysaccharide materials, secreted by bacteria and al­
gae, that both sequester ions and isolate the
microorganisms from the water column (Wetzel and
Allen, 1970; Allen, 1971; cf. review of Burkholder,
1996). Accumulated detrital particles and precipitated
calcium carbonate crystals, as well as the glycocalyx
materials, enhance nutrient enrichment by adsorbing
phosphorus, ammonium, and various organic sub­
stances (Fig. 19-3). Nutrients may be assimilated,
sometimes with the aid of excreted enzymes such as
phosphatases (sfc), utilized, and released via leaching,
excretions, secretions, or cell lysis by the benthic algae
(A) (Fig. 19-3). Epiphytic microfauna and macrofauna
can release phosphatases and nutrients during feeding
LEAF EPIPHYTE MATRIX WATER
SURFACE (1-2000 p.m thickness) COLUMN
FIGURE Ì9-3 Diagram of the supply of nutrients (Nw, such as
organic and inorganic forms of carbon, phosphorus, and nitrogen) to
benthic algae and other microbes within a periphyton matrix on a
substratum, in this case a submersed macrophyte leaf. Arrows indi­
cate routes of nutrient cycling form the substratum and the water
column, which represent the two major external sources of nutrient
supply to the periphytic matrix. (See text for explanation of relation­
ships and symbols.) (From Burkholder, 1996.)
and excretion (e.g., fecal pellets (FP) with viable algae
and bacteria that have become nutrient-enriched during
passage through the animal gut, nutrient waste prod­
ucts, and dead microflora and other organic detrital
particles).
Other nutrient-sequestering or -releasing materials
include inorganic calcium carbonate (Ca) that is precip­
itated by photosynthetic processes and siliceous frus-
tules of dead diatoms (Si), organic debris (e.g., recently
dead algae and animals, Or), and microbially derived
hydrated glycocalyx/mucopolysaccharides (Gl) (Fig.
19-3). The microflora and fauna can also be colonized
and attacked by fungi, especially when moribund, and
this process would result in nutrient remineralization
or release. Some algae and bacteria are directly adnate
to and in contact with the leaf or other substratum sur­
face. Other microflora are loosely attached in the over-
story matrix, and some have stalks or other attachment
structures to the substratum (Fig. 19-4).
Insight into the community structure of epiphytic
microflora of submersed macrophytes can be gained
from electron photomicrographs 2 of a typical associa­
tion (Fig. 19-4). The surface structure of the epiphytic
community (Fig. 19-4A) indicates the manner in which
the loosely woven diatomaceous component is held in
place by a stranded matrix formed largely from gelati­
nous stalks of mucoid substances (Fig. 19-4B), which
2
The scanning electron photomicrogrraphs were kindly provided by
Dr. B. R. Allanson University, South Africa; some are from his in­
vestigations reported in Allanson (1973).
 /. Attached Microbes and Algae of Littoral Regions

FIGURE 19-4 The structure of a microfiorai community upon the macroalga Chara from Wytham
Pond, Oxford, England. (A), Surface view of microflora on a stem (X75); (£), The epiphytic community
after exposure to pH 4.5 to remove calcite deposits, showing the dominant diatom Achnanthes minutis-
sima and mucoid membranes attached to the wall of the host plant (X500); (C), Intimate association
between the diatom component and supporting mucoid matrix, calcite deposits removed (XlOOO); (D),
transverse feeding tracks left by nymphs of the baetid mayfly Cloeon dipterum (X500); (£), a chironomid
larva, found enclosed in fronds of Chara, which may have been feeding in this position (X90).
(Photographs courtesy of B. R. Allanson, 1973. From Allanson, B. R.: Fine structure of the periphyton of
Chara sp. and Potamogeton natans from Wytham Pond, Oxford, and its significance to the macrophyte
periphyton metabolic model of R. G. Wetzel and H. L. Allen. Freshwater Biol. 3:535-541, 1973.)
584 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton

/ \ > y Bacteria

« A & J ? " Enzyme

^ W Fluxes

X/^jlA Polysaccharide

^ 7 Product

i V ^ A Substrate

(9 W01V

-7—7—7—r—7—7 7—7—r—r-7 7—7- /

FIGURE 19-5 Conceptual model of the structure and metabolic fluxes within periphyton
communities and from or into microchannels of the polysaccharide matrix and the overlying
water. (See text; modified slightly from Lock, 1993.)

in places extends as a fragmented membrane above the
deposits of calcium carbonate covering the cell wall
(Allanson, 1973; Roos et al., 1981). While some algae
(diatoms and cyanobacteria) and heterotrophic bacteria
are loosely associated within and on the calcite and
mucoid complex, others penetrate through the complex
to the macrophyte itself and attach themselves directly
along its entire surface or by means of simple or
branched mucilagenous stalks. Much of the matrix is
associated with the mucopeptide cell walls of the epi­
phytic bacteria, algae, and cyanobacteria, an associa­
tion that is lost in the techniques used to prepare these
scanning electron photographs; this matrix can be seen,
however, in transmission electron microscopy.
Most of this relatively rich community of mi­
croflora epiphytic upon macrophytes is destined to
become detritus. Massive accumulation rates on the
supporting plants Chara and Potamogeton (Allanson,
1973) and differences seen in the fine structure of the
epiphytic-carbonate-mucoid complex between parts of
the plant as it grows and provides new surfaces for
colonization indicate that little of the community is uti­
lized by grazing animals. In places, however, evidence
for grazing occurs (Fig. 19-4 D,E).
Periphyton structure is envisaged to consist of mi­
crobes embedded within the polysaccharide matrix
made from material secreted by bacteria and algae (Fig.
19-5). The polysaccharide matrix is potentially perme­
ated by microchannels that may act as conduits in
which diffusion of organic and inorganic nutrients is
faster than through the polysaccharide matrix (Lock,
1993; Costerton et ai, 1994; DeBeer et al, 1994;
Wimpenny and Colasanti, 1997). The size of these mi­
crochannels varies greatly but is commonly in the range
of 5 - 5 0 /xm, and they permeate the microbiota and
matrix in a dendritic, likely fractal pattern (Fig. 19-6).
The amount of the polysaccharide matrix and likely the
size of these microchannels is influenced by external
factors. For example, microchannel size is increased in
the presence of high dissolved humic substances and ul­
traviolet irradiance (Wetzel et al, 1997, unpublished).
Fluxes of nutrients and dissolved gases from and to
the overlying water and among microbial components
within the periphyton would be faster in the liquid of
 /. Attached Microbes and Algae of Littoral Regions 585

FIGURE 19-6 Fluorescent microspheres dispersed within microchannels of a lentie periphyton community at
one focal plane about 75 /xm below the surface-overlying water boundary. Black areas are bacterial and algal
cell clusters within extracellular polysaccharide matrix. (E. Espeland and R. G. Wetzel, unpublished.)

the microchannels than through the matrix itself. Pho-
tosynthetic products of algae released intercellularly
can be used by bacteria or may diffuse into the chan­
nels and to the overlying water. Reciprocally, bacteria
secrete organic micronutrients (e.g., vitamins), C 0 2 ,
and enzymes intercellularly that may persist in the ma­
trix for some time before being assimilated by algae or
other microbes or diffusing from the matrix. Mem­
brane-bound or -released extracellular enzymes may
hydrolyze dissolved organic matter (DOM) released
from other microbes, especially algae, or from DOM or
particulate organic matter (POM) adsorbed from the
overlying water. These hydrolyzed products can then be
assimilated by microbes, adsorbed by the polysaccha­
ride matrix, or be diffused into the microchannels or
overlying water.
The polysaccharide matrix permeated with mi­
crochannels forms a physical medium in which diffu­
sion is much slower than in the overlying water. A
conceptual model, depicted in Figure 19-7, indicates
the periphyton matrix attached to and overlying the
substratum (Riber and Wetzel, 1987). In the interstitial
water of the matrix, the concentration of a nutrient
(Cm) will be the net effect of numerous factors,
586 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
PLANKTONIC
ALGAE,
ALGAE AND
BACTERIA]
BACTERIA
U IT:H
I 3~
B However, at low flow rates, much of the water mass
BOUNDARY PERIPHYTON
LAYER MATRIX
FIGURE 19-7 A conceptual model of nutrient (P) exchange
between the organism in a periphyton matrix, the boundary layer,
and the bulk water in which the nutrient availability is affected by
exchange with planktonie organisms {a, upper). Nutrient concentra­
tion gradient ( ) between the bulk-water concentration (Q,) and
the periphyton matrix concentration (Cm). The concentration at the
matrix surface is C0 (b, lower). (Modified from Riber and Wetzel,
1987.)
including uptake and release by algae and bacteria and
adsorption by particles. Cm will vary somewhat as a
function of periphyton depth due to biological stratifi­
cation and exchange processes. The concentration at
the matrix surface is denoted C0. In the bulk water, the
nutrient or gas concentration (Q,) is correspondingly
determined by the activity of the plankton. The ex­
change of nutrient or gas between the two systems will
be through the diffusive boundary layer. The mass flux
through the boundary layer, N, is given by the general
equation
N = h(Cb - C0)
where b is the boundary-layer mass transfer coefficient,
which depends on hydrodynamic conditions, including
currents and turbulence in the bulk water (Chap. 7),
and the geometry of the substratum and periphyton
community structure. In some cases, h can be estimated
by hydrodynamic calculations (Skelland, 1974). Since
the net flux depends on the difference between bulk
water and matrix concentrations, flux may go in either
direction and can change rapidly with differences in
metabolic conditions. When both systems are limited
by nutrients and the concentrations are low, the net
flux will be small or even zero.
The structure of the periphyton community can
also influence transfer flux rates. Because of the uneven
development and distribution of periphytic microbiota,
some groups of organisms project upward and contain
valleys in between. This increased roughness can theo­
retically increase turbulence as water flow velocities in­
crease over the communities (e.g., Nikora et al., 1997).
passes over the community with little turbulence be­
tween the high and low points of the community (Riber
and Wetzel, 1987).
E. Growth-Regulating Resources
A number of consumable resource requirements in­
fluence the metabolism, growth, production, and ex­
ploitative competition among periphytic communities.
Important distinctions are needed among (a) external
resources in the overlying and surrounding medium,
such as light and nutrients, (b) internal resources that
are obtained from abiotic or biotic sources within the
substrata on which the periphyton communities are at­
tached, and (c) internal recycling within periphyton
among algae and associated microbiota, as summarized
later (pp. 593-594). All of these parameters are sum­
marized in a comparative manner in Table 19-1.
1. Habitat Space
The availability of space for colonization is essen­
tial and markedly affects the composite productivity of
the periphytic communities. As will be emphasized in
the discussion on microspatial community structure
and on comparative productivity later, the periphytic
communities attached to surfaces (e.g., rock, and
sediments) that are relatively fixed in area available for
colonization and development can rapidly be limited
by space when other growing conditions are good.
Although these communities can project somewhat
above the surface, and certain stalked and filamentous
algal forms do so (e.g., Hoagland et ai, 1982), the
communities readily become compacted and stratified
with steep gradients of light attenuation, redox, and ac­
cumulated products of fermentation (Wetzel, 1993a).
In contrast, periphyton growing epiphytically on sub­
mersed macrophytes have manifold increased surface
TABLE 19-1 Summary of C o m m o n Responses of Epilithic, Epipelic, and Epiphytic Autotrophic Microbiota to D o m i n a n t Physical, Chemical, and Biotic
Resource Parameters*

Environmental parameter Epilithic Epipelic Epiphytic

Physical
Water movement High in rivers and upper littoral
areas; molar abrasion high
Substrata Stable at low-to-moderate
water velocities
Temperature Often, marked seasonal and
diurnal fluctuations
Light
a. Quantity Steep seasonal changes, especially
low in canopied streams; steep
exponential declines with depth
b. Quality Selective attenuation by water column
Habitat available Moderate; sorting by wave action
and flowing water; sets particle
size and surface area
Chemical-biotic
General conditions Usually oxic; low nutrients
Inorganic nutrients
a. Phosphorus Low, often restrictive
b. Nitrogen Low, often restrictive
c. C 0 2 (HCO3-) Usually adequate to high
d. Others Usually adequate
Organic substrates/nutrients
a. Organic micronutrients Low, but variable with season in lakes
and floodplain inundation in rivers
b. Heterotrophy Algal heterotrophy low or absent;
bacterial heterotrophy low
to moderate
Primary productivity Low to moderate
Symbiotic interactions among Low
microbes and substrata
a
Greatly modified from Wetzel (1983b).
High —> low in depth gradient;
decreasing with depth
Unstable; subject to frequent
disturbance
Decreasing with increasing depth;
higher and variable in epilimnion,
low and more stable in metalimnion
High —> low in depth gradient; rapid
decrease within sediments
Steep selective attenuation of red and
blue spectra within periphyton and
within sediments
Low; essentially two-dimensional
Reducing but diurnal oxic; high nutrients
Very high from interstitial waters
Very high from interstitial waters
Very high from sediment metabolism
High
Very high from sediment metabolism
Algal heterotrophy potentially moderate,
likely low; bacterial heterotrophy
very high
Low
Moderate to high
High exchange in water column; low
exchange within dense submersed
macrophtye stands
Stable in position, but changing with
growth and senescence; often
increasing seasonally
Commonly high in shallow areas
and changing widely seasonally
Moderate to high; decreasing with
depth but often increasing
seasonally as submersed macro-
phytes develop upward into
water column
Selective attenuation in water column
and by pigments within periphyton
communities
High, particularly among submersed
macrophytes; projection into water
column, three-dimensional
Oxic, with diurnal variations
Low, variable; some from macrophyte
Low, variable; some from macrophyte
Low to high; much internal recycling
Low; likely much internal recycling
Low, high microbial competition,
much internal recycling
Algal heterotrophy low; bacterial
heterotrophy high
High
High to very high
588 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton

Epipelic

\ \ \ \ \ \ \
Organic Sediment + Sediment + POM +
Sediment POM Detritus Submersed Macrophytes

Spatial
Volume

Surface
Area

Oxic/Anoxic Oxic/Anoxic Oxic

FIGURE 19-8 Transition of substrata surface area for attachment of periphyton from a predomi­
nantly two-dimensional spatial habitat through increasing surface area of particulate organic matter
(POM) detritus to a fully three-dimensional spatial habitat of surface area of submersed aquatic
plants.

area as the substrata becomes three-dimensional and
projects upward into the water column and enhanced
light field (Fig. 19-8). Not only does the surface area
available for colonization increase exponentially but
the spatial volume increases greatly with much greater
exposure of the communities to largely oxic water col­
umn conditions (Fig. 19-8).
Analogous conditions occur in running waters.
Although submersed macrophytes are much less well
developed in streams and rivers (cf. Chap. 18), large
woody debris often constitutes significant particulate
organic debris (cf. Chap. 21) and can provide appre­
ciable surface area for colonization by periphyton.
Large woody debris tends to be moved downstream
during flooding events considerably less than does fine
particulate matter. In addition, stones and other parti­
cles tend to organize in clusters during high water ve­
locity events and flooding in streams where a large an­
choring stone (an obstacle clast) and smaller stones
lying against the upstream face of the clast (the stoss)
provide a hydraulic shelter for accumulation of
smaller particles behind in the wake tail (Fig. 19-9).
The surface area of the smaller rocks is increased con­
siderably in comparison to large rock surfaces and
shifts upward in a modest three-dimensional manner.
Although the abrasive and export actions of flooding
events often greatly reduce the abundance of attached
algae, these microform bed clusters of hydraulic
refuges can provide increased substrata area and
support appreciably greater algal periphyton (e.g.,
Biggs et al., 1997; Francoeur et al., 1998). Among
epipelic algal communities on organic sediments, how­
ever, a very small size of sediment grains, particularly
below 125 /im, reduces the sites for microalgal com­
munity development (Cahoon et al, 1999). With the
shift toward a two-dimensional configuration, algal
biomass is reduced and declines with the increasing
percentage of very fine particles.

Single stoss clusters
obstacle
stoss clast
Flow
obstacle
stoss clast
FIGURE 19-9 Microform bed clusters of sediment particles downstream of a large
anchoring obstacle clast and smaller stones (the stoss) lying against the upstream face
of the clast. (From Francoeur et al, 1998.)
2. Nutrient Availability and Utilization
from the Overlying Water
The physiological requirements and growth re­
sponses of attached algae are similar to those of phyto-
plankton, already discussed at length (cf. Chap. 15).
Nutrients can be obtained by diffusion into the com­
munities from the overlying water or from below from
the substratum, which may be living or senescing (e.g.,
macrophytes), dead (organic detritus), or relatively in­
ert, such as rock. Nutrient availability is determined by
hydraulic conditions at the boundary layer that influ­
ence the thickness of the diffusive layer, the concentra­
tions of compounds dissolved in the bulk environment
of the surrounding water, and the metabolic activity of
the attached organisms for utilization or production of
the compounds.
At the macrogradient level of influence of nutrient
concentrations of the overlying water on the develop­
ment and production of periphyton communities, nu­
merous studies have demonstrated that enrichments of
nutrients, particularly P and N, in the overlying water
commonly result in enhanced growth of attached algae
on many different substrata. Examples are many.
Growth responses of natural epiphytic communities of
submersed macrophytes of an oligotrophic lake of
Michigan were compared to that of another area of the
littoral in which nutrients were administered to simu­
late release from macrophyte tissue (Moeller et al.,
1998). Epiphytic growth increased immediately where
phosphate was released above the sediment, and after
10 weeks a 40-fold increase of epiphytic algal biomass
occurred at the center of the plot as compared to bio-
mass immediately outside of the m 2 -plots. Whole-lake
/. Attached Microbes and Algae of Littoral Regions 589
Multiple stoss clusters
fertilization experiments with P and N in a shallow,
subarctic Swedish lake resulted in massive increases in
phytoplankton (Bjςrk-Ramberg and Aneli, 1985). The
resulting competition for light resulted in precipitous
declines to less than half of the periphyton primary
production to the total lake photosynthetic production.
In unfertilized lakes, high periphyton productivity was
maintained and contributed 7 0 - 8 3 % of the total lake
primary production. In habitats with relatively abun­
dant nutrient concentrations, dense phytoplankton can
shade periphyton development severely as the attached
communities shift from nutrient to light limitations
(e.g., Hansson, 1992).
Nutrient enrichment of the overlying water can
also lead to marked changes in species composition of
periphyton communities. For example, nitrogen enrich­
ment led not only to an increase in epilithic algal abun­
dance but to a shift from a diatom/N 2 -fixing cyanobac-
teria-dominated community to one dominated by
diatoms (Hawes and Smith, 1992). Where combined ni­
trogen insufficiency is maintained, N 2 fixation by at­
tached cyanobacteria appears to be a successful strategy
for survival in N-deficient environments on both a sus­
tained and on a seasonal basis (Reuter et al, 1983,
1986). However, species composition of algal periphy­
ton is often relatively unresponsive to small changes in
the nutrient concentrations and dynamics in the overly­
ing water (e.g., Cattaneo, 1987; Pringle, 1987; Riber
and Wetzel, 1987; Fairchild and Sherman, 1993;
Neiderhauser and Schanz, 1993). Such recycling allows
a short-term (days to weeks) functional separation of
the metabolism within the periphyton from the nutrient
concentrations in the overlying water, which indicates
590 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
the importance of intensive recycling of nutrients within
the microbial community. Although that separation
cannot persist indefinitely, it represents a marked adap­
tive advantage in which inputs from the overlying water
can be directed largely to new net growth and produc­
tion to augment the recycling occurring within the com­
munity between algae and bacteria (Wetzel, 1993a; see
later discussion). If enhanced nutrient concentrations
are sustained over long periods of time, distinct species
change in the attached algal communities. For example,
along a long gradient of nutrient enrichment as a point
source to a wetland of the Everglades, periphytic algal
growth decreased with greater distances from the point
source of nutrients and eutrophic diatom species were
replaced by oligotrophic diatom species as the total
phosphorus concentrations decreased below ca. 15 jug
liter" 1 (McCormick et al, 1996, 1998). Because of light
limitations by the dense macrophytes under the eu­
trophic conditions of the gradient, periphyton produc­
tion was greater in the oligotrophic sites despite the
reduced phosphorus availability.
Rates of diffusion from the overlying water to the
periphyton communities are influenced by the thickness
of the boundary layer as well as solute or gas concen­
tration gradients. Because the thickness of the bound­
ary layer, within which fluxes occur by diffusion, de­
creases with increasing current flow across the surface,
the boundary layer is less in rivers than in lakes. Re­
gardless of flows, nonturbulent boundary layer thick­
nesses cannot be reduced below ca. 10 ^m (Raven,
1970; Smith and Walker, 1980; Koch, 1990). In pro­
tected areas, such as in backwater areas, refuges, or
within aquatic plant beds of both standing and flowing
waters, very much lower water current velocities and
much greater boundary layer thicknesses (10 2 -10 5 /xm)
occur (e.g., Losee and Wetzel, 1993; Sand-Jensen and
Mebus, 1996; Stevens and Hurd, 1997). In addition,
the thicknesses of the microbial communities of stand­
ing waters are very large, often several millimeters or
even centimeters, than in streams. Water movements
reduce the thicknesses appreciably by the sloughing off
of cells and export downstream (cf. Stevenson, 1996b).
Within limits, increasing current enhances nutrient
uptake rates and as a result often also photosynthesis,
respiration, cell division, biomass, and productivity (cf.
many references cited in Stevenson, 1996b). Obviously,
water movements across periphyton interfaces would
replenish nutrient concentrations in microzones within
the boundary layers where they have been reduced by
metabolic uptake and chemical reactions. The advan­
tage accrued by increasing water velocities is highly
variable, but the saturating current velocity for algal
assemblages in many flowing habitats is in the range of
4 to perhaps 20 cm s _1 . As periphyton densities and
community thicknesses increase, collective metabolism
per unit area and growth rates decline, and nutrient de­
mand increases. Depending on the architecture of the
attached communities, reliance on the nutrients from
the overlying water stabilizes and there is generally a
shift to greater internal recycling of nutrients and gases
within the periphyton community (Fig. 19-10) (Wetzel,
1993a). As communities develop and increase in thick­
ness, instability can occur and cells and portions of the
community may slough off. Alternatively, very dense
biomass development of filamentous algae, such as
Cladophora, requires water currents, either unidirec­
tional in streams or multidirectional as in wave-turbu­
lent areas of lakes, presumably because of the inade­
quacy of internal recycling within the community.
With increasing current velocities, shear stress re­
sulting in drag on periphyton causes losses and export
of cells downstream (cf. Stevenson, 1996b). In addi­
tion, at high current velocities and small boundary lay­
ers, the metabolism of attached algae can be reduced
for reasons not well understood. Regenerated nutrients
and extracellular enzymes may be lost across the inter­
face to the moving water before they can be effectively
utilized.
Attached benthic algal and microbial communities
themselves, as a whole, are not porous, but rather are
relatively impervious to throughflow. In contrast, many
of the substrata upon which the algae grow, such as
sand and organic particles, are very porous to intru­
sions from surface flows and from groundwater
sources. The scale of this movement, however, is much
larger than that of the metabolic environment of the in­
dividual cells of the attached microbial communities.
An important distinction is that although the substrata
may be porous, the periphyton communities are not;
within the periphyton, fluxes of nutrients are by diffu­
sion along concentration-mediated gradients. Those
gradients are highly dynamic as mediated by the photo-
synthetic and respiratory metabolism of the microbiota
and, in the case of macrophytes, the living substrata
upon which the attached community may be growing.
3. Nutrient Interactions of Attached
Algae with Substrata
Attached microbial communities are well posi­
tioned to utilize nutrients and organic compounds re­
leased from the substratum upon which they are grow­
ing as well as from the water column. Marked
differences in the species and quantities of epiphyte
communities have been observed on natural as opposed
to artificial plants in oligotrophic and mesotrophic
habitats (Cattaneo, 1978; Cattaneo and Kalff, 1978;
Eminson and Moss, 1980; Gough and Gough, 1981;
Burkholder and Wetzel, 1989a,). Artificial nutrient

BIOMASS
( )
TIME
INTENSITY OF
INTERNAL
NUTRIENT
RECYCLING
TIME
FIGURE 19-10 Successional development of, and increased nutrient recycling within,
microbial communities on substrata (see text). (From Wetzel, 1993a.)
enrichment by experimentally following biomass differ­
ences on nutrient-diffusing artificial substrata in com­
parison to nutrient enrichments of the overlying water
column have demonstrated that nutrients from the
substratum are effective in increasing growth as well as
altering community species composition (Fairchild
et al, 1985; Carrick and Lowe, 1988; Pringle, 1990).
Although the capability for nutrient utilization is obvi­
ous from these studies, the question still remains about
the utilization rates and significance of nutrient acquisi­
tion from the substrata under natural conditions.
Despite the early negativism that periphytic com­
munities were obtaining essentially nothing nutrition­
ally from the substrata, modern experimental evidences
indicated quite the contrary—many periphytic com­
munities are highly dependent upon the substrata for
mineral and organic nutrients, particularly in olig-
otrophic and mesotrophic environments where the
greatest periphyton productivity occurs. The influence
of the supporting macrophytes in determining the epi­
phytic algal community is greatest in infertile waters.
As the surrounding water becomes more fertile, exter­
/. A ttached microbes and Algae of Littoral Regions 591
PENETRATION
(DIFFUSION)
RATES
(—)
nal environmental factors influence epiphytic growth
more than do inputs from the host macrophyte.
These relationships are well demonstrated among
epiphytic algae and bacteria. In addition to the very
large surface areas for colonization and retention of
algae and other microbes, submersed macrophytes also
provide significant sources of nutrients from both living
as well as senescing tissues (Harlin, 1973; Moeller
et al, 1988; Burkholder and Wetzel, 1990; Burkholder
et al, 1990; Burkholder, 1996; Wetzel, 1996). The nu­
trients from the substrata internally supplement those
diffusing into the attached communities from the water
within and passing through the littoral zone. Complex
nutrient interactions exist among algal species. For
example, certain algal species growing adnate to the
macrophyte can obtain > 6 0 % of their phosphorus
from the macrophytes (Fig. 19-11). Algae near the
outer portion of the community obtained less phospho­
rus from the macrophyte, but nonetheless significant
quantities emanated from the plant. Even when phos­
phorus concentrations are very high in the water,
some phosphorus, and presumably other nutrients, is
592 19. Land-Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton

RATIO OF TRACK DENSITIES if)

WATER

GOMPHONEMA

MOUGEOTIA

LYNGBYA
PERIPHYTON
NAVICULA

ACHNANTHES

LARGE DIATOMS

* en OB
o o o oo oo o o O O

LEAF PROPORTION OF P FROM HOST (%)

FIGURE 19-11 Sources of phosphorus within an epiphytic community on the submersed
macrophyte Najas flexilis. Epiphytic algal taxa are arranged according to increasing proportion
of phosphorus received from the host plant. The relation between r {upper) and the proportion
{lower) is implicit in the dual scaling. A 90% confidence interval was calculated from raw data
(open box) and corrected data (bar). (From Wetzel, 1990a, based on data from Moeller et al,
1988.)

obtained from the macrophyte, simply because diffu­
sion rates from the water into and within the complex
epiphytic community are too slow to meet high meta­
bolic demands. Little phosphorus incorporated into the
periphyton passed to the macrophyte (Moeller et al,
1988).
An additional example is the previously discussed
(see Chap. 14) results of Jorgenson (1957), who found
that diatoms epiphytic on the reed Phragmites com­
peted with plankton for silica of the water early in the
major growing season. Later in summer and fall, appar­
ent utilization by the diatoms of silica from the Phrag-
mites stems gave them a competitive advantage over
planktonie forms (see Fig. 14-23). Certain other littoral
algae also have high requirements for silicon (e.g.,
Moore and Traquair, 1976; Hooper-Reid and Robin­
son, 1978). Spring and autumnal population maxima
are common in epiphytic diatom communities on sub­
mersed macrophytes and have been correlated with nu­
trient availability (e.g., Siver, 1978). Benthic microalgae
are also important regulators of silica fluxes; epipelic
diatom utilization can reduce fluxes to the overlying
water and potentially influence phytoplankton growth
and species composition (Sigmon and Cahoon, 1997).
As macrophytic tissue senesces, much of the phos­
phorus is translocated to rooting tissues. However, an
inward swelling and disorganization of the epidermal
cells of the macrorphyte occur (Rogers and Breen,
1981). Bacterial degradation penetrates and slowly de­
grades epidermal cell walls. This loss of cellular in­
tegrity of the leaves results in leaching from the leaves.
Nutrients and dissolved organic compounds are readily
utilized by periphytic microflora,'which tend to develop
profusely during autumn and winter periods in temper­
ate regions. For example, more labile amino acids were
readily assimilated and retained within periphyton
communities to a greater extent (ca. 43%) than were
more recalcitrant dissolved organic substrates leached
from decaying emergent macrophytes (3-4%) (Bicudo
et al, 1998).
Microdistribution of species and groups of epilithic
algae is correlated directly with differences in microdis-
tributions of rock facies and differences in solubility of
specific elements from the rock (Smith et al, 1992).
Mineral nutrient (Fe, Si, and trace elements) can leach
from the rock substratum and be utilized by the at­
tached microflora with alterations in microdistributions
of algal species. The distribution of epipsammic algae is
influenced and their productivity often increased by nu­
trient content and microscale differences in diffusion
and microflows among interstitial waters through
sandy sediments, as well as sand grain morphology and
topography (Krejci and Lowe, 1986, 1987). In both
streams and lakes, hyporheic and groundwater flows
can enhance nutrient availability and productivity of
attached algae, often in very patchy areas of the ben­
thic materials where local variations of inflows enter
the stream or lake (e.g., Hagerthey and Kerfoot, 1998).
Epipelic algae growing upon organic sediments of­
ten develop into dense communities, both loosely at­
tached and in dense, matlike aggregations. Often these
communities are several millimeters in thickness. Even

in relatively sparsely developed communities on sedi­
ments, photosynthesis of the epipelic algae and com­
munity respiration can markedly affect nutrient fluxes
from the sediments to the overlying water (reviewed by
Burkholder, 1996; Wetzel, 1996). Fluxes are affected
by metabolic alterations of redox and coupled chemical
mobilities and by direct assimilation and utilization.
The importance of epipelic photosynthesis, oxygen,
and pH in a microzone at the sediment-water interface
and bacteria to the mobility of phosphorus from the
sediments and to nitrogen fluxes from the sediments
was discussed in detail earlier (Fig. 13-8; pp. 215, 253,
and 602). The production of oxygen and penetration
of oxygen into the sediments can result in supersatu­
rated oxygen conditions of interstitial water and rapid
shifts, in a matter of minutes, in redox potentials be­
tween highly reducing to highly oxidized conditions.
Fluxes of phosphorus from the sediments to the overly­
ing water are nearly totally suppressed under these oxi­
dizing conditions, as well as from microbial utilization
(Carlton and Wetzel, 1988). Such marked diurnal fluc­
tuations in oxygen and other chemical microgradients
have been shown in various epipelic loosely attached
algae and mat-type algal communities, (e.g., Jorgensen
et ai, 1979, 1983; Hansson, 1989). Attached benthic
algae also scavenge nitrogen as NH 4 —N from intersti­
tial waters of sediments (Jansson, 1980).
It should be recalled that the exchange of nutrients
and metabolic products is not all from the macrophyte
or detritus to the attached periphyton community.
Much discussion (summarized later) has evolved on the
negative effects of dense periphyton communities on
the physiology of the supporting macrophytes, such as
light reduction and especially inhibition by competition
for nutrients and gases from the surrounding water. As
we have seen in the discussion of the macrophytes
(Chap. 18), the rooted macrophytes rely heavily on nu­
trient acquisition from the sediments and on internal
recycling of oxygen and C 0 2 within the intercellular
gas channels. Nonetheless, it is likely that gases, partic­
ularly C 0 2 , produced within the periphyton communi­
ties diffuse to the macrophyte for assimilation. Simi­
larly, it is probable that certain nutrients recycling
among periphyton constituents also diffuse along con­
centration gradients to the macrophytic cells at the in­
terface with the periphyton. Other than the studies of
Moeller et al. (1988), there are few experimental
demonstrations of such fluxes, which is a fertile area of
investigation.
4. Nutrient Recycling within the
Periphyton Community
The relatively significant hydraulic isolation by dif­
fusive boundary layers of periphytic communities from
/. Attached Microbes and Algae of Littoral Regions 593
the overlying water, as well as the close physical prox­
imity of their cells, indicates a tight physiological cou­
pling between attached algae and bacteria. Much of the
evidence for this interdependent metabolic relationship
is circumstantial. Dissolved organic matter released
from stream benthic algae during photosynthesis was
taken up by periphytic bacteria, and attached bacterial
productivity was positively correlated with the release
of dissolved organic matter from benthic algae (Haack
and McFeters, 1982; Kaplan and Bott, 1989). The pro­
ductivity of bacterial periphyton may depend to a
greater extent upon external dissolved organic sub­
strates in early stages of colonization and then shift to
a greater reliance on organic substrates from algal pro­
duction as the communities thicken and become more
complex in structure (cf. Sobczak, 1996). More direct
experiments in which photosynthesis of attached algae
was inhibited under controlled conditions demon­
strated that periphytic bacterial productivity depended
on algal photosynthesis (Neely and Wetzel, 1995).
Either algal exudates of organic matter stimulated bac­
terial production or photosynthetic oxygen increased
aerobic bacterial activity, but in either or both cases a
direct metabolic coupling was indicated.
Attached bacterial metabolism may also enhance
algal metabolism and growth in periphyton, as has
been shown often in mixed cultures, for a number of
potential reasons (e.g., Lange, 1971; Haines and
Guillard, 1974; Mouget et ai, 1995). Enhancement of
algal growth can result from bacterial reduction of oxy­
gen tension that could reduce photorespiration or from
increased production of C 0 2 or growth factors such as
vitamins that the algae cannot produce. Phosphorus
uptake kinetics of periphyton, for example, were found
to be acutely limited by boundary-layer mass transfer
and a power function of flow velocity (Riber and
Wetzel, 1987). Kinetic calculations based on turnover
measurements indicated that internal recycling of phos­
phorus and recycling from the boundary layer, rather
than external uptake, accounted for most phosphate
turnover within intact periphyton. Under optimal
conditions, it was estimated that the turnover time of
phosphorus was so rapid that phosphorus was recycled
between algae and bacteria every 15 s. Similarly,
denitrification rates by denitrifying bacteria within epi­
phytic periphyton are high in the dark and on senescent
macrophyte tissues but inhibited by oxygen produced
by the periphytic algae or the living macrophyte tissues
(Eriksson and Weisner, 1996). Analogous results were
found for the effects of light in epipelic periphyton,
where photosynthetic oxygen of algal photosynthesis
reduced the rate of denitrification within the microbial
community precipitously (Risgaard-Petersen et ai,
1994).
594 19. Land- Water Interfaces: Attached Microorganisms, Littoral Aigae, and Zooplankton
Recently, efforts have been made to evaluate en­
zyme activities produced by periphyton communities as
an estimate of potential capacities to hydrolyze organic
substrates for specific nutrients, such as phosphorus or
nitrogen, and energy. Many assays estimate enzyme ac­
tivity by enzymatic degradation of a nonfluorescent
substrate into a highly fluorescent product in the water
surrounding the periphyton (e.g., Chappell and Goul-
der, 1992, 1994; Jones and Lock, 1993; Scholz and
Boon, 1994). Because enzymes can occur and function
within and throughout the attached microbial commu­
nity, their synthesis and use can be only partially re­
lated to enzyme concentrations in the overlying water.
Moreover, the enzymes may be hydrolyzing organic
substrates of the substratum to which they are at­
tached. The lack of explicit evaluation of sources and
of where the enzymes are being produced and utilized
by the use by the attached microbial communities con­
founds how they are functioning. Recent substrate as­
says allow evaluation of individual insoluble fluores­
cent products at the cellular levels for specific enzyme
activities such as phosphatase and protease (Huang
et al, 1998; Francoeur and Wetzel, 2000).
Negative interactions can also occur. For example,
competition for the same nutrients, well known among
the plankton, likely operated among attached micro-
biota as well. Algae and bacteria may produce sub­
stances that are inhibitory to the growth of the com­
petitors. Because of the large number of species present
in periphyton communities, it is probable that both
positive and negative responses are occurring simulta­
neously in the same community.
Aquatic fungi, primarily hyphomycetes, are abun­
dant constituents of periphyton on and within sub­
mersed leaves, wood, and other organic detritus (e.g.,
Bΰrlocher, 1992; Shearer, 1992). Fungal growth and
productivity usually far exceed that of attached bacte­
ria on these substrata (cf. Chap. 21). However, hy­
phomycetes are rare on nonorganic substrata such as
rocks. Even though fungi utilize simple, soluble organic
molecules, they likely compete ineffectively with bacte­
ria that have high affinities for these substrates
(Suberkropp and Klug, 1976). However, there is some
evidence for mutualistic fungal-bacterial interactions
even at the species-specific level (Bengtsson, 1992).
5. Light Availability and Utilization
Light attenuation in relation to periphyton photo­
synthesis must be examined at two spatial scales,
namely, with depth in the water column before reach­
ing the periphyton and at the microscale within peri­
phyton communities. The selectively spectral diminu­
tion of light with depth has been discussed at length in
Chapter 5 (pp. 56-60), where it was shown that dis­
solved organic matter selectively removes large por­
tions of the ultraviolet and blue portions of the spec­
trum and the water molecules per se selectively attenu­
ate the infrared and red portions of the spectrum.
Particulate matter such as phytoplankton is relatively
unselective but can attenuate total photosynthetically
active radiation appreciably when in high densities.
In very clear lakes, light can penetrate well below
the common lower limit (ca. 10 m) of growth of vascu­
lar aquatic plants and support appreciable periphyton
communities on rocks, sediments, and particulate detri­
tus. For example, in Lake Tahoe of California—Nevada
light adequate to support photosynthesis of epilithic
periphyton can penetrate to 60 m (Loeb et al, 1983).
Although littoral attached communities may require
modest light (ca. 200 fxmol irT 2 s_1) for photosynthetic
light saturation (e.g., Turner et al, 1983; Hill, 1996),
net photosynthesis occurs at much lower intensities,
such as in the range of 5 - 2 5 |jimol m - 2 s _1 (Wetzel
et al, 1984; Lorenz et al, 1991). As discussed in the
descriptions of community and productivity dynamics
later, depth and turbidity-associated alteration of light is
clearly a factor regulating development of periphyton.
Experimental analyses of light interactions under nat­
ural conditions are few but corroboratory (e.g., Hudon
and Bourget, 1983; Marks and Low, 1993).
Light obviously affects rates of photosynthesis and
thus influences primarily growth. Often, estimates of
algal periphyton are made by evaluating biomass, com­
monly as chlorophyll a per unit area. Instantaneous
biomass does not necessarily estimate growth rates
over time, however, where mortality from disturbance,
grazing, pathogens, and other factors is significant. In
headwater streams where streambank vegetation is
abundant and shades the channel, light reduction can
markedly suppress periphyton photosynthesis. Algal
biomass is often 5-fold times higher in unshaded sites
in comparison to those with full tree canopy, particu­
larly when grazing pressure is low or moderate (many
references cited in Hill, 1996). In both lakes and
streams, light- or nutrient-enhanced primary produc­
tion that is not expressed in increased periphyton bio-
mass when grazing is heavy is instead reflected in in­
creased grazer growth or densities (Hill et al, 1995;
Moeller ζtf tf/., 1998).
Light is attenuated very rapidly within periphyton
communities, but the community structure is heteroge­
neous and spatially variable on substrata. As a result,
light gaps occur, and variable light attenuation occurs
among cell aggregations, calcium carbonate crystals,
and weakly pigmented algal cells and through dead di­
atom frustules that act as light conduits (Losee and
Wetzel, 1983). Different species dominating the
epiphytic community can also influence the nature of

cellular structure and relative penetration of light into
the communities as a whole (Dodds, 1992).
In addition to reductions in quantity, epiphytic
microbiota can also modify severely light quantity and
quality reaching the supporting macrophyte. It was
demonstrated experimentally that it is primarily the pho-
tosynthetic pigments of algae and cyanobacteria that at­
tenuate selectively light in the red (ca. 675 nm) and par­
ticularly the blue (ca. 430 nm) portions of the spectrum
(Losee and Wetzel, 1983; Jorgensen and Des Marais,
1988; Plough et al., 1993). Heterotrophic bacteria, dead
diatom frustules, and carbonate crystals were nonselec-
tive. The recent development of fiber-optic microprobes
(100 to <50 firn in size) now allow detailed examina­
tion of light quantity and quality within periphytic com­
munities with minimal disturbance (e.g., Jorgensen and
Des Marais, 1988; Dodds, 1989; Plough et al, 1993;
Kuhl and Jorgensen, 1994). Backscattering of light
within these communities increases the total scalar irra­
diance to which embedded algal cells are exposed.
Algae of periphyton communities are relatively
well protected by carotenoid pigments against high
light intensities, and little photoinhibition has been
demonstrated (cf. review of Hill, 1996). Algal produc­
tivity and photosynthetic oxygen production of peri­
phyton were significantly reduced by small enhance­
ments of ultraviolet irradiance, which in turn reduced
the bacterial productivity coupled to rates of algal pho­
tosynthesis (Kahn and Wetzel, 1999). Microscale re­
ductions in water level of only a few millimeters, as is
common in shallow littoral and wetland areas on a
daily basis, can result in marked increases in UV irradi­
ance intensities and alterations in periphytic metabo­
lism. There is some evidence (Bothwell et al., 1993;
Francoeur and Lowe, 1998) for long-term adaptation
by periphytic diatoms in streams, however, where ini­
tially inhibitory effects of UV on growth were reversed
after several weeks of species succession.
F. Growth-Regulating Mortality and Losses
In addition to growth regulation and exploitation
competition for resources, a number of processes con­
tribute to mortality, losses, and interference competi­
tion: predatory mortality, largely by grazing inverte­
brates and fishes; natural physiological senescence,
death, and population turnover; diseases and viral
mortality; and physical disturbances from water move­
ments and substrata instabilities. Each is briefly sum­
marized here and in Table 19-1.
1. Grazing Mortality of Periphyton
Ingestion of microbial communities attached to
surfaces has many ramifications for nutrient cycling,
/. A ttached Microbes and Algae of Littoral Regions 595
productivity, and energy flows in inland waters. Several
aspects need to be considered, namely: (1) direct inges­
tion and mortality of periphyton; (2) release of incom­
pletely metabolized dissolved and particulate organic
detritus by the grazers; (3) effects of grazing mortality
on the relative productivity of the periphyton commu­
nities and the substrata (e.g., living macrophytes) sup­
porting the communities; and (4) nutrition and energy
derived by the grazing animals (see Chap. 22).
The growth and productivity of the sessile attached
microbiota, particularly epiphytes on submersed por­
tions of macrophytes, can be affected by grazing activi­
ties of animals (e.g., insect larvae, snails, crayfish, tad­
poles, and certain phytophagous fishes) (Flint and
Goldman, 1975; Mason and Bryant, 1975; Bowen,
1978; Eichenberger and Schlatter, 1978; Kitchell et al.,
1978; Hunter, 1980; Hagashi et al., 1981; Power et al.,
1985; Lamberti et al., 1987, 1992; Brςnmark, 1989;
Feminella et al., 1989; Feminella and Resh, 1991;
Steinman et al., 1995; Steinman, 1996). In certain
cases, when the epiphytic algal biomass is low, growth
and productivity per unit area of the attached algal and
bacterial community can be stimulated (turnover rates
increased) by moderate levels of grazing. Moderate
grazing could improve access of algae to nutrient and
light resources from the overlying water and enhance
algal growth as a result. For example, in grazing of
stream periphyton communities by snails, the physical
disruption and release of nutrients by ingestion and
partial digestion can accelerate nutrient regeneration to
the overlying water that is normally retained and
recycled within the periphyton community. Similar re­
sults were found among grazing oligochaetes and snails
on epiphytic periphyton of a lake (Kairesalo and
Koskimies, 1987). From a quarter to over half of the
phosphorus ingested as food was released from the ani­
mals through defecation and excretion.
Heavy grazing pressures often result in reductions
in overall periphytic biomass or productivity under
the commonly used experimental conditions of high
grazer density without natural predation pressures
upon the herbivores. However, many factors influence
the attached microbial-grazer interactions (cf. Wetzel,
1983b; Steinman, 1996), including (a) herbivore type;
(b) periphyton density and stage of development; (c)
nutrient availability (concentrations, gradients, and wa­
ter movements at the interface); (d) light quantity and
quality; and (e) past disturbance frequency. Clearly, in­
creased nutrient availability and light commonly have
positive effects and grazing has negative effects on bio-
mass and productivity of periphyton (e.g., Hart and
Robinson, 1990; Rosemond, 1993; Rosemond et al.,
1993; Moeller et al., 1998). Compensatory responses
of both periphyton and grazing communities are
596 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
marked and rapid, and as a result of these variable
impacts, patterns resulting from the effects of herbivory
are difficult to delineate. Extreme care is needed in ex­
trapolation of grazing studies under intensively con­
trolled laboratory conditions to field situations (cf.,
e.g., Fuller et al, 1998). Although the instantaneous
biomass of periphyton may be reduced by grazing,
often the productivity of the periphyton community is
enhanced by the constant cropping of portions of the
attached communities. Little if any effects of macroin-
vertebrate grazing could be detected on the detachment
and redistribution of attached bacteria (Leff et al,
1994).
Very little evidence exists for true species-specific
selectivity of attached microflora by grazers. Some ex­
perimental studies suggest that algivorous protozoan
herbivores and oligochaete worms select prey diatoms
on the basis of size and certain species (Bowker et al,
1985; McCormick, 1991). Grazing macroinvertebrates
are generally omnivorous and randomly ingest algae,
bacteria, particulate detritus, and inorganic deposits
(e.g., CaC0 3 ). The structure of benthic microbial com­
munities, although highly variable, can influence graz­
ing efficacy. For example, prostrate species are attached
adnate to the substratum, upright or stalked species
form a middle level, and filamentous species often
emerge from the community to an upper level
(Hoagland et al., 1982). Mayfly larvae with gathering
collector-feeding structures tend to feed along the outer
layers among the loosely attached portions of the peri­
phyton. Snails and caddisfly larvae use rasping and
scraping mouth parts and are adapted to feed among
the low-profile, adnate, attached periphyton. As a re­
sult, larger diatoms (>20 ^tm) may be more effectively
removed by these herbivores than small green algae
and cyanobacteria (Cuker, 1983). Herbivore abun­
dance may not be in synchrony with seasonal varia­
tions in periphyton production, which may result in
apparent minimal grazing impacts. Low-to-moderate
grazing usually results in no appreciable changes in at­
tached algal diversity, but intense grazing pressure can
reduce diversity (e.g., Lowe and Hunter, 1988; Mulhol-
land et al., 1991). Certain fatty acid components of
attached algae are distinctly inhibitory to grazing inver­
tebrates (e.g., LaLonde et al, 1979), and fatty acid
composition of the periphyton can be altered by graz­
ing (Steinman et al., 1987). Whether this response is an
allelochemical induction, as occurs among the phyto-
plankton (cf. Chaps. 15 and 16), is unclear.
There is some evidence that grazing mortality of
periphyton is a greater percentage of total death and
turnover of attached communities in stream ecosystems
than in standing waters. Most of the microflora at­
tached to macrophytes and other substrata is not con­
sumed by animals, but instead enters detrital decompo­
sition pathways within the ecosystem (cf. Chap. 23).
2. Disturbance
Disturbance to the habitat and general milieu of
periphyton communities is relative in relation to physi­
cal disruptions, such as by water movements, and ex­
ternal impacts such as chemical alteration (e.g., acidifi­
cation) or pollution. The latter topic is a subject of its
own and is extensively treated in pollution and water
quality literature. For example, much of the saprobic
system of evaluating water quality is based on indicator
species of attached algae and other microbiota under
different conditions of pollution (e.g., Slΰdecek, 1973).
In lakes with relatively stable water levels, periphy­
ton is well adapted to living in shallow areas of turbu­
lence from wave actions. When periphyton that devel­
oped in relatively quiescent, nonturbulent habitats are
subjected to unusual water turbulence, such as that as­
sociated with an episodic storm event, loosely attached
microbiota can be dispersed. Stalked diatoms and simi­
lar microbes attach tightly to substrata but are suffi­
ciently flexible to tolerate appreciable water movement
(Cattaneo, 1990; Hoagland and Peterson, 1990).
In reservoirs, and to a certain extent also in wet­
lands, water levels can fluctuate widely. Obviously, the
lowering of the water level and desiccation of periphy­
ton communities suppresses growth and increases mor­
tality. Although many diatoms and cyanobacteria are
capable of surviving long periods of desiccation, others
such as desmids cannot (cf. review of Goldsborough
and Robinson, 1996). Fluctuating water levels in reser­
voirs often expose unconsolidated sediments to wave
turbulence and result in resuspension and high turbid­
ity. Similarly in shallow ponds and wetlands, high wind
activities can increase turbidity and reduce light pene­
tration. Suppression of photosynthesis and growth of
periphyton accompanies such light reductions. If tur­
bidity is short-lived, however, nutrient availability can
be increased from the sediment disturbance and result
in a positive effect on growth. Conversely, epidemic de­
velopments of the exotic zebra mussel (Dreissena poly-
morpha) in lakes can reduce planktonie turbidity by
feeding activities and result in improved underwater
light distribution (Nalepa and Schloesser, 1993). In­
creased periphyton growth can occur both in response
to enhanced light but also because of the greatly in­
creased surface area for colonization by the profuse
development of mollusk shells.
In river ecosystems, the physical effects of turbu­
lence and drag on cells of periphyton can be severe in
removal of loosely attached cells and exporting them
downstream and in disturbing substrata (Peterson
et al, 1994; cf. review of Stevenson, 1996b). Although

attached microbial communities are well adapted to
water movements, particularly up to about 15 cm s _1 ,
at sudden spates of greater velocities, the export of cells
increases precipitously. Conversely, immigration of cells
from upstream and colonization on substrata decrease
as current velocities increase.
Complex indirect effects on periphyton communi­
ties of fluctuations in current velocities in rivers occur
(Stevenson, 1996b). The size of sediment particles
moved is proportional to current velocities (cf. pp.
97ff), and increasing currents can move substratum
and attached microbes with devastating effects from
abrasion and redistribution to a less suitable habitat
downstream (buried, deeper or shaded areas, et cetera).
The time between spate events of sufficient magnitude
to move substrata is important. If sufficiently long to
allow reasonable development of the microbial com­
munities prior to the next major disturbance, overall
community productivity can be quite high. Frequent or
unusually high hydrographic events can markedly sup­
press periphyton productivity.
Changes in current velocities, particularly strong
episodic events, can also modify the distribution and
movement of herbivorous benthic invertebrates and
fish, particularly in central areas of stream channels of
fast currents (Poff and Ward, 1992; Hart and Finelli,
1999). Any disturbance of the sediments, such as from
nesting of insects or fish, similarly affects the develop­
ment of periphyton and alters the spatial distribution
of attached microbiota in streams.
3. Other Losses
Losses of natural communities of attached micro-
biota by natural senescence and death, by parasitism
particularly by viruses, and by disease are poorly
known. As among the phytoplankton and bacterio-
plankton, nonpredatory losses are certainly significant
and likely constitute over half of the natural mortality.
This area is a fertile field for study.
G. Community Analyses and Seasonal Dynamics
The development of attached microbial communi­
ties on a new surface passes through several stages.
Firstly, accrual occurs with colonization of the substra­
tum and subsequent growth in approximately an expo­
nential sigmoid curve (Fig. 19-10). The duration of the
accrual phase toward maximum biomass varies with
conditions, of course, but is commonly in the range of
one to 2 weeks under natural conditions. A shift then
occurs to a predominance of internal nutrient recycling
and a greater balance between growth and loss
processes by death from parasitism, disease, and graz­
ing as well as sloughing and export of cells from the
/. A ttached Microbes and Algae of Littoral Regions 597
community (Fig. 19-10). Growth is approximately bal­
anced where high productivity is maintained photosyn-
thetically by internal recycling of nutrients and gases
and utilization of external resources from the overlying
water and counterbalanced by losses and disturbances.
Quantitative evaluations of attached benthic algal
populations are much more difficult than qualitative
floristic analyses. Recognition of the various habitats
and their associations is a problem common to both
analyses which is accentuated by ineffective sampling
techniques that are difficult at best. It is difficult to sep­
arate epipelic algae from sediments, but separation is
necessary for accurate enumeration. Phototactic re­
sponses of the algae can assist in this separation; alter­
natively, one can use other biomass methods such as
pigment content (correcting for pigment degradation
products common to sediments). Quantitative sampling
of epilithic and epiphytic algal /cyanobacterial popula­
tions is even more difficult, but a number of devices
and procedures have been devised (see the reviews of
Slΰdeckovΰ, 1962; Lowe and Laliberte, 1996; Steven­
son, 1996; Wetzel and Likens, 2000) that permit some
degree of quantification. The problems of quantitative
sampling of attached algae are further compounded by
the settling of casual species originating from the
plankton and metaphyton into the benthic populations,
especially during winter. Only detailed sampling of the
different communities combined with metabolic assays
of growth can resolve this problem.
1. Use of Artificial Substrata
Because of extreme habitat and community hetero­
geneity, artificial substrata of uniform composition and
colonizable area are commonly used to estimate colo­
nization and growth characteristics of attached algae.
In addition to examination of microbiota on natural
substrata, artificial substrata that have been used in­
clude glass slides, glass fiber filters, concrete blocks,
rocks and rock plates, sand, various plastic and metal
plates, and wood.
There are several restrictions inherent in the use of
artificial substrata. Marked differences in colonization
rates and biomass accrual have been found in relation
to the position of the supported substrata and their lo­
cation within the aquatic system. For example, verti­
cally positioned plates on which sedimenting organisms
from the plankton or metaphyton could not accumu­
late contained less biomass but more realistically simu­
lated population characteristics found on natural
substrata than did those positioned horizontally (e.g.,
Castenholz, 1961; Pieczyρska and Spodniewska, 1963).
The influence of water movement or simply the process
of retrieving the slides following incubation can lead
to significant losses of attached microflora. Some
598 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
organisms will not adhere to artificial substrata such as
glass until early successional forms have colonized the
substratum, which may or may not occur within the
period of incubation (e.g., Blinn et al., 1980). Appar­
ently glass is not seriously selective for the attachment
of diatoms (Patrick et al., 1954), although diatoms can
utilize some of the silica from the glass. Grazing can
lead to alterations of attached communities that may
influence the results, depending on whether the ques­
tions being addressed concern specific attached flora or
the entire attached community.
Some investigators have positioned artificial sub­
strata in the pelagic zone of lakes or main flow of
streams quite removed from sites of natural substrata.
Although these analyses may have some value in a rela­
tive sense, such as in evaluating responses to inorganic,
organic, or acidic toxicants in different water types or
venues (Genter, 1996; Hoaglund et al., 1996; Planas,
1996), they are of relative or little value in evaluating
natural attached communities.
The most serious criticism that can be directed
against studies using artificial substrata centers on the
implicit assumption that any metabolite, inorganic or
organic, of the living or nonliving substrata has no
appreciable effects on the metabolism and growth of
the attached community. Similarly, it is assumed that
the metabolism of the attached microfiorai community
has no reciprocal effects upon the substratum. Recent
evidence for such synergistic effects is overwhelming
that much more than a passive relationship exists
among the attached microbiota (see discussion on pp.
590-594).
With these thoughts in mind, the difficulties of
quantitatively evaluating natural population growth on
natural substrata become apparent. Even though the
mutual metabolic relationships are real, especially
among epiphytic algae and the supporting macro-
phytes, measuring the effects of the heterogeneous at­
tached populations on the highly variable substrata of­
ten exceeds the capacities of existing methods. The
problem is a technical one that must be approached
without the use of artificial substrata. Alternatively,
when used critically, artificial substrata can be a mean­
ingful tool for the approximate estimation of biomass
accrual of many attached microorganisms. Much of
our existing information on these communities is based
on analyses using artificial substrata. Only a few inves­
tigations have addressed the in situ rates of algal pro­
ductivity by means of metabolic techniques.
2. Examples of Population Fluctuations
The detailed investigations of the population dy­
namics of epipelic algae of several lakes of the English
Lake District (Round, 1957a-c, 1960, 1961a,b) serve
to illustrate several characteristics of these populations,
as well as the potential spatial, temporal, chemical, and
biotic factors affecting growth. Diatoms completely
dominated the epipelic community, and patterns of dis­
tribution could be discerned on the basis of general
chemical features of the sediments and overlying water.
Other algal groups were less well represented. The
Volvocales were very sparse, and the Chlorococcales
were represented only by the genera Pediastrum and
Scenedesmus. Although not abundant, the desmid flora
was richer in species than other groups. Euglenoids
were much more common on more organic-rich sedi­
ments. Little correlation was found between the growth
cycles of the epipelic and planktonie cyanobacteria,
and in some lakes, a conspicuous development oc­
curred on the sediments but not in the plankton.
Epipelic cyanobacteria developed equally well in alka­
line, neutral, and slightly acidic waters.
In general, a larger diatom biomass corresponded
to a higher organic-matter content of the sediments,
and growth was better on sediments with more leach-
able silica. Moderate organic-matter content of the
sediments favored cyanobacterial populations, while
low populations were associated with sediments of
very high and very low organic-matter content. Popu­
lations of the poorly represented Chlorophyceae and
the flagellated forms were distinctly greater on organic-
rich sediments. Although little correlation was found
between population numbers and sediment content of
sodium, potassium, iron, or manganese, the diatom,
cyanobacterial, and flagellated algal populations were
directly correlated with calcium content. Algal growth
was also greater on sediments with high phosphate
content.
Although population numbers of epipelic algae ex­
hibited large variations from lake to lake, and between
sites within lakes, and with depth, certain consistent
patterns emerged. The main growth period of epipelic
diatoms and cyanobacteria of lakes of this moderate
temperate region3 was in the spring, commencing
about February (Fig. 19-12). Except for the wave-ac­
tive shallow zone (0-1-m depth), population numbers
were relatively constant on sediments between 1- to
6-m depths; below this depth, numbers decreased pre­
cipitously to practically nil at depths greater than 8 m.
The growth of the dominant benthic diatom, Tabellaria
flocculosa, was shown experimentally to be largely re­
lated to light intensity, which decreased rapidly with in­
creasing depth (Cannon et al., 1961; Hillbricht-
Ilkowska et al., 1972). Strictly phototrophic diatoms
are more sensitive to light than cyanobacteria, whose
3
Ice cover is rare and usually short-lived, typically only a few days in
duration.

3000 H
2000
1000 H
m
Nj T' rD I J ' F ' M ' A ' M ' J ' J ' ,
1948 1949
FIGURE 19-12 Seasonal cell counts of epipelic diatoms {left) and cyanobacteria (right), in which all
the depth stations are added together for each sampling date in the photosynthetic zone ( 1 - 6 m) of
Lake Windermere ( ) and Blelham Tarn (
depth distribution usually extends considerably deeper
than that of the diatoms. The general seasonal biomass
of epipelic algal populations in the photosynthetically
illuminated zone generally followed the curves of inci­
dent light and water temperature.
In streams, light availability frequently limits ben-
thic algal growth (e.g., Whitton, 1975; Wetzel, 1975b;
Marker, 1976; Aizaki, 1978; Biggs, 1996; Hill, 1996).
Light availability can be altered markedly by seasonal
changes in the leaf canopy of deciduous trees adjacent
to the stream. The succession of species within the
overall annual cycle of epipelic algae is a much more
elusive and complex matter. Among planktonie popula­
tions of algae, discussed in some detail in Chapter 15,
the changes in physical and chemical parameters, par­
ticularly those associated with periods of circulation in
stratified lakes, are very large and can influence domi­
nance and competitive abilities of the species. The
sudden collapse of populations at certain times of the
year is related, in part, to these "shock" events of
disturbance. 4 Epipelic populations tend to occur largely
above the metalimnion, so the effects of disruption of
stratification may be less on these populations than
among the plankton. The seasonal succession of at­
tached algal species is, however, just as pronounced as
succession among the planktonie species (Round,
1972).
No temperate epipelic algal species is known to
persist as a numerically dominant species over an entire
year. Specific epipelic algal populations tend to increase
quite rapidly and then decline equally rapidly. Often,
several successive species associations tend to dominate
during an annual cycle, each phasing in to the next
from live cells that have remained in the habitat for
some time after cell division has ceased. The substrata
provide innumerable microhabitats, certainly many
more than exist under planktonie conditions of the
pelagic zone. Therefore, one would expect a large
number of coexisting species in the attached algal com-
4
A concept discussed by Round (1971).
/. Attached Microbes and Algae of Littoral Regions 599
S ' O ' N'
), England. (Modified from Round, 1961b.)
munity at almost any time of the year. Sampling
techniques that tend to aggregate algae from many dif­
ferent microhabitats can obscure this distribution.
Annual and seasonal cycles of epipelic algae are
marked and complex (e.g., Round, 1964a; Ilmavirta,
1977; Sheath and Hellebust, 1978; Romagoux, 1979).
Diatom growth in lakes often commences in early
spring and reaches maximum cell numbers in April to
May in the temperate zone, after which a decline
occurs in midsummer prior to a smaller autumnal
peak that is over by November. Although this pattern
is similar to that of planktonie species, the epipelic
algal pattern occurs more slowly than that found
among planktonie algae. On shallow sediments, the
epipelic algal populations tend to exhibit early winter
and spring maxima, followed by a later midsummer
maximum.
Spring maxima are common among attached algal
populations of streams, although these populations are
subject to irregular decimation and disturbance by
moving substrata during spates (see, e.g., Douglas,
1958; Sand-Jensen et ai, 1988). In woodland streams,
the seasonally changing light passing through the ter­
restrial canopy can shift the productivity pattern from
one that is autotrophic in the spring to one of essen­
tially heterotrophic dominance later in the season
(Kobayasi, 1961; Biggs, 1996; and also discussion in
Chap. 22). That seasonal pattern may also reflect a sea­
sonally in herbivory by aquatic invertebrates, which
tends in the temperate zone to be greater in the autumn
and early winter. Where disturbance is common, partic­
ularly from spates and flood events, seasonal patterns
with a spring maximum are frequently interrupted. Im­
mediately after a flood event, periphyton may recover
rapidly and achieve maximum biomass during a win­
dow of time when invertebrate grazer densities are low
because invertebrate reproduction and recolonization is
much slower (Grimm and Fisher, 1989; Power, 1992;
Peterson, 1996).
The seasonal population dynamics of epiphytic al­
gae growing on submersed portions of macrophytes are
600 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton

CS
I
E
O)

A S O N D F M A M
1968 1969
FIGURE 19-13 Chlorophyll a concentrations, extrapolated upward to g m~2 of the littoral zone on
the basis of estimated surface areas of the macrophytes, of algae attached to artificial substrates in dense
stands of the littoral zone dominated by (A), the emergent bulrush Scirpus acutus, and (£), the submer-
gents Najas flexilis and Chara, Lawrence Lake, Michigan. Note the marked differences in the scales of
the ordinate in g m~ 2. (After Allen, 1971.)

much more involved because the surface area available
for colonization and growth is continually changing as
the macrophytes grow, senesce, and enter detrital
phases. Computations of the population changes of the
total epiphytic algal community are rare, but changes
obviously are quite different among different support­
ing macrophyte communities (Kowalczewski, 1975a,b;
Cattaneo and Kalff, 1980; Muller, 1996). For example,
changes in the biomass of attached algae associated
with a zone of the emergent bulrush Scirpus acutus
were more than an order of magnitude lower and out
of phase with those of algae attached to substrates in a
shallow zone dominated by submersed plants (Najas
flexilis and Chara) (Fig. 19-13). Detailed analyses were
made of the population and community dynamics of
epiphytic algae and cyanobacteria on leaves of the sub­
mersed sedge Scirpus subterminalis in a hardwater tem­
perate lake (Burkholder and Wetzel, 1989a). Epiphytic
diatoms comprised a mean of 90% of the total epi­
phytic algal biovolume, whereas cyanobacteria con­
tributed a mean of 88% of the total algal-cyanobacte-
rial cells. Epiphytic cyanobacteria were a negligible
portion of the algal biomass except during autumn,
when they contributed 40% of the total. However,
cyanobacteria were estimated to produce > 5 0 % of the
total algal carbon (Fig. 19-14).
Part of the reason that the productivity of epiphytes
is so high is their persistence within the water column
throughout much of the year (Fig. 19-15). Most sub­
mersed macrophytes are perennial plants; many species
grow or persist in a dormant or "evergreen" condition
for much of the year (cf. Chap. 18). The above-
sediment biomass of submersed macrophytes commonly
reaches a maximum in the spring-early summer period
and gradually declines as resources are diverted to root­
ing tissues. An appreciable macrophyte biomass and
surface area can persist all year in subtemperate regions
and even under ice in temperate regions.
Epiphytic biomass and productivity tend to be rela­
tively constant throughout the year (Fig. 19-15). Com­
petition among epiphytic algae and phytoplankton for
nutrients can reduce epiphytic development in the
midyear period. This late spring maximum decline po­
tentially results from increasing nutrient limitations,
temperature, and grazing pressure. Epiphytic growth,
particularly by cyanobacteria, often increases markedly
in late summer and autumn. At this time, lake mixing
occurs during autumn, nutrient supplies increase in the
water, temperatures decline, macrophyte senescence
accelerates, and epiphytic diatom/cyanobacteria popu­
lations increase (Fig. 19-15). Diatom productivity is
particularly high in winter and spring periods.
Most of the nutrients of actively growing macro­
phytes are obtained from the sediments. As was
demonstrated, most (95-99%) of phosphorus, for ex­
ample, is obtained from sediment interstitial water and
is retained within the plant and recycled repeatedly (cf.
Chap. 13, Fig. 13-9). Nutrients from littoral water are
very actively assimilated by the loosely attached epi­
phytic periphyton, incorporated into the periphyton,
 /. Attached Microbes and Algae of Littoral Regions

DIATOMS

BLUE-GREENS OTHER

100
is

^UN 1 JUL ! AUG ' SEP  OCT ' NOV ' DEC ' JAN ' FEB ! MAR ' APR
1983 1984
FIGURE 19-14 Organic carbon content of epiphytic algae and cyanobacteria (blue-greens) on api­
cal portions of the submersed sedge Scirpus subterminalis in Lawrence Lake, southwestern Michigan.
(From Burkholder and Wetzel, 1989a.)

SUBMERSED
MACROPHYTES

Above-ground
Macrophyte
Biomass

Spring Summer Autumn Winter Spring

Nutrient DOM Release

t i
Diatoms Diatoms
Competition Nutr. Release
Periphyton with Warm, BQs
Phytoplankton Epiphytes
Increasing

Epiphyte
Biomass -
Productivity

FIGURE 19-15 Generalized relationship of epiphytic biomass and productivity in relation to variations in
aboveground biomass of submersed macrophytes (see text for discussion). P = perennial and A = annual
plants; BG = cyanobacteria. (From Wetzel, 1990a.)
602 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
and intensively recycled. Relatively little of these nutri­
ents pass to the macrophyte. The periphyton, rather
than the submersed macrophytes, functions as the pri­
mary scavenger for a limiting nutrient such as phos­
phorus from the water. During dormancy phases and
senescence of aboveground foliage, much of the critical
nutrients is translocated to rooting tissues. Losses from
the leaves are readily utilized by the periphytic commu­
nity, which tends to develop profusely during autumn
and winter periods. As the senescing macrophytes with
their epiphyte communities collapse to the detrital mass
near the sediments, much of the nutrients is incorpo­
rated into the sediments and is actively retained and re­
cycled by the sediment epipelic microflora (Fig. 13-9).
The fluxes from the sediments to overlying water are
actively influenced by photosynthesis of epipelic algae
within the microzone at the sediment-water interface
and by the bacterial metabolism below the interface
(see Chaps. 12 and 13).
The general assumption that the chemistry of the
overlying water has a direct controlling effect on
epipelic algae has not been verified experimentally. If
buried in the sediments, the algae may also be exposed
not only to lower intensities of light but also to anaero­
bic conditions within the sediments. Many benthic al­
gae can survive anaerobiosis for several days and may
retain considerable photosynthetic potential in the ab­
sence of oxygen (Moss, 1977). For those species
adapted to epipelic existence, the proximity to the
totally different chemical milieu of the interstitial water
within and immediately adjacent to the sediment-
water interface can give them a distinct advantage that
is quite unrelated to chemical events occurring in the
overlying water. For example, the biomass of epipelic
algae commonly increases as the organic carbon, nitro­
gen, and phosphorus content of the sediments increases
(Skorik et al., 1972). A large portion of the ammonia
nitrogen of interstitial water of sediments was found to
be assimilated by benthic algae (Jansson, 1980). Dis­
solved organic nitrogen compounds released to the
overlying water originated largely from the algae. Ni­
trogen fixation by epipelic, as well as epiphytic,
cyanobacteria and heterotrophic bacteria is common
(Finke and Seeley, 1978; Moeller and Roskowski,
1978) and, as indicated earlier (Chap. 12), can consti­
tute a significant input of combined nitrogen to some
lakes. Yet the epipelic forms are not completely exempt
from the characteristics and events of the overlying wa­
ter. For example, a high content of dissolved organic
matter or a seasonally variable development of plank-
tonic algae or of macrophytic vegetation populations
would markedly affect the quality and quantity of light
reaching the sediments, the thermal regime of the sedi­
ments, water movements near and along the sediments,
et cetera. Although it is intuitively apparent that chang­
ing events in the overlying water can influence the
species succession and productivity of epipelic algae,
studies of these interactions are essentially nonexistent.
The whole area of investigation is uncharted and diffi­
cult but is one that is approachable by the systematic
application of modern research techniques.
II. METABOLIC INTERACTIONS
IN THE LITTORAL REGIONS
A. Relationships between Algae and
Bacteria of Periphyton
The macrophytes release large quantities of both
inorganic compounds (e.g., oxygen, carbon dioxide,
phosphates, silica, et cetera) and organic compounds
secreted during active photosynthesis and released by
autolysis during senescence into the immediate prox­
imity of adnate epiphytic microflora and littoral wa­
ters (e.g., Howard-Williams et al., 1978; Siver, 1980;
cf. Chap. 18). As we have seen, this proximity alone is
conducive to transfer and exchange of nutrients (P0 4
and C0 2 ) between the epiphyte and the supporting
plant. In hard waters, precipitation of calcium carbon­
ate is induced by photosynthetic activity (Chap. 11) to
form a matrix intermixed with the microflora and mu-
coid substances (predominantly polysaccharides and
peptides). The epiphytic bacteria actively utilize, in
part, organic substrates released by the macrophytes
and algae. Dissolved organic compounds not utilized
by this association and not adsorbed within or to
surfaces of precipitating calcium carbonate, enter the
pool of littoral dissolved organic matter for further
degradation by bacteria (Fig. 19-16). In turn, epiphytic
bacteria produce C 0 2 and certain organic micronutri-
ents (e.g., vitamin B12) (cf. Wetzel, 1969, 1972), that
can serve as growth factors for the macrophytes or
algae, or both. Photoassimilative active uptake of
labile organic substrates has been demonstrated for a
submersed angiosperm in axenic culture and for a
species of the macroalga Nitella (Smith, 1967; Wetzel,
unpublished).
There is evidence to support the conclusion that
most phytoplanktonic algae cannot actively augment
photosynthesis by heterotrophic utilization of organic
substrates when in competition with bacteria that ac­
tively assimilate the same substrate (e.g., Mayfield and
Inniss, 1978; cf. Chaps. 15 and 17). The immediate
juxtaposition of attached algae to the metabolically ac­
tive area of a living plant and bacterial concentrations
can give them a distinct competitive advantage over
their planktonie counterparts living in a habitat where
 LITTORAL PELAGIAL
ALL0CHTH0NOUS
MATERIALS

CARBONATE-MUCO-ORGANIC COMPLEX]
eoa

]FARTICULATE COMPLEXING OF INORGANICS

CaCOj EPIPHYTIC INTERACTIONS

UJ ALGAE , I
I
ORGANOTROPHY
_i_
X HIGH PHOTQ-
LITTORAL DIRECT UTILIZATION
CL DOM EXCESS DOM (REFRACTORY)
INTERACTIONS DOM
O POOL  INDIRECT REGULATORY
tr POOL
o EFFECTS

<
EPIPHYTIC J GROWTH FACTORS

BACTERIA

ACTIVE - PASSIVE RELEASE OF DOM

\PART/CULATE\
^ADSORBED, . CaC03
^ DOM
CO2 .

DOM
\EPIPEUC ALGAL AND
/
BACTERIAL COMPLEX /CaC03
- RESOLUBILIZATION

\ \ \ \ \
SEDIMENTS
\ \ \ \ \
FIGURE 19-16 Diagrammatic representation of major metabolic pathways and interactions in the littoral zone of a typical lake; see text for discus­
sion. DOM = dissolved organic matter; PS = photosynthesis. (Modified from Wetzel and Allen, 1970.)
604 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
nutrients are much more dispersed (see, e.g., the studies
of Allen, 1971).
Analogous interactions certainly exist within the
epipelic associations of algae and bacteria. Unfortu­
nately, even less is k n o w n about the qualitative and
quantitative metabolic interrelationships of these at­
tached forms and their substrate than is k n o w n about
the epiphytic microflora. Potential sources of inorganic
nutrients and labile dissolved organic substrates are
likely to be greater under reducing conditions of the
s e d i m e n t - w a t e r interface than at the surfaces of
macrophytes.
Dissolved organic substrates emanating from lit­
toral sources or from the drainage basin are degraded,
flocculated, and adsorbed as they travel to the pelagic
zone (cf. Chaps. 18, 2 0 , and 23). The rates and kinds
of "processing" that occur en route are highly variable
and depend upon the dynamics of seasonal and indi­
vidual differences in the physical and chemical parame­
ters of lakes. The littoral region can be viewed as func­
tioning as an effective but selective metabolic sieve or
sink for certain dissolved organic c o m p o u n d s and inor­
ganic nutrients from littoral and external sources to­
ward the pelagic zone (e.g., Howard-Williams and
Lenton, 1975; Klopatek, 1975; Lee et al, 1975;
Gaudet, 1977, 1978, 1979; Howard-Williams and
Howard-Williams, 1978; Mickle and Wetzel, 1978a, b,
1979; Prentki et al, 1978; Stewart and Wetzel, 1981a;
Wetzel, 1990a, 1992). During this transport, the more
easily degradable organic substrates tend to be decom­
posed in the littoral zone and c o m p o u n d s of greater re­
calcitrance (i.e., slower turnover rates) tend to move to­
w a r d the open water. Therefore, even though the
amounts, rates of utilization, and fate of inorganic and
organic c o m p o u n d s released from the littoral zone vary
seasonally and differ from lake to lake, their direct and
indirect effects on the metabolism of the pelagic mi­
croflora can be great in m a n y lakes.
B. Effects of Light Availability
Within dense stands of emergent macrophytes, the
rapid attenuation of light plays a major role in the re­
duction of photosynthesis of littoral algae. For exam­
ple, in reed stands of Phragmites, Straskraba and
Pieczyρska (1970) found a rectilinear relationship be­
tween the percentage transmission of light through the
emergent parts of the reed and shoot density. As much
as 9 6 % of the incoming radiation was removed above
the water, whereas the density of the stand had little
further influence on the light availability under water.
The rather low light intensities occurring in reed
stands, especially those of an average or high density,
substantially lowered photosynthesis and biomass of
TABLE 19-2 Effect of Increased Light Availability on
Photosynthetic Activity of Phytoplankton and Attached Algae
in a Dense Stand of Phragmites communis before and after
Removal of Plant Shoots, Smyslov Pond, Czechoslovakia,
in September*
With Phragmites
Phragmites cut
0 cm 30 cm 0 cm 30 cm
Phytoplankton (mg 0 2 liter-1 day"1)
Gross production 0.14 0.06 7.9 3.0
Respiration 0.17 0.78 2.6 1.5
Attached algae
Gross production 3.1 8.7
(mg 0 2 dm -2 day-1)
^From data of Straskraba and Pieczyρska (1970).
phytoplankton entering the stands from the pelagic re­
gion. Photosynthetic activity of attached algae is simi­
larly reduced in these dense stands. Cutting experi­
ments showed a large increase in photosynthetic
activity of each algal group, and the increase was di­
rectly proportional to the percentage improvement of
light conditions (Table 19-2). In less dense stands of
emergent plants, as, for example, in low-growing
sedges, light reduction is not as serious, but a strong
limitation of photosynthesis of phytoplankton still has
been observed (Straskraba, 1963). Some decomposi-
tional organic c o m p o u n d s released from the plants
were also believed to contribute to this reduction.
Another striking example of the importance of the
shading of light from periphyton by emergent macro­
phytes was determined in the Everglade wetlands of
Florida (Grimshaw et al, 1997). Photosynthetically ac­
tive radiation reaching the periphyton communities
was reduced by only 3 5 % in the more open sloughs of
the emergent sawgrass (Cladium mariscus) but by 8 5 %
or more in dense stands of cattail (Typha domingensis).
Photosynthetic rates of periphytic algae and cyanobac-
teria in sawgrass habitats were reduced by about 3 0 %
from those in openwater slough habitats; the net pro­
duction rates of periphyton communities in the cattail
communities were reduced by 80 ± 8 % of rates in the
open communities.
Light reduction by a seasonal development of an
emergent macrophyte canopy can cause a seasonal re­
duction in the epiphytic periphyton as well. For exam­
ple, the productivity of epiphytic algae on Equisetum
was very high in early summer but declined during the
summer as shading by the macrophytes increased
(Kairesalo, 1984). Herbivory by snails also increased as
the summer season progressed.

Light availability can also be reduced by abiotic
factors at intermittent intervals and have marked
effects on periphyton productivity. For example, algal
biomass epiphytic on floating meadows of aquatic
plants in an Amazon floodplain lake was severely
reduced by inorganic turbidity imported by river
water (Engle and Melack, 1993). Nonetheless, high
turbidity impacted composite phytoplankton growth
more severely, and as a result epiphytic algal produc­
tivity per unit area was much higher than that of the
phytoplankton.
G. Attached Algae as a Source of Phytoplankton
The concept that littoral benthic algae can give
rise to plankton algae emerged many years ago. It was
assumed that plankton algae formed resting spores
that overwinter in or upon the sediments and that
under conditions favorable to germination and popu­
lation development, algae on the sediments served
as the inoculum for the phytoplankton. In moderate-
size to large lakes, there is no evidence for any
conspicuous buildup of algae on the sediments before
a plankton bloom, but rather only afterward when
the dead plankton settle out onto the sediment
(Round, 1964).
An alternative concept is that planktonie popula­
tions are always present in the water, although in ex­
tremely low concentrations. These few remnants of past
populations can then serve as the inoculum for a rapid
population increase under favorable growing conditions.
This situation seems to be the case for most species.5 In
one of the better studies of algae, resting spores of the
diatom Asterionella formosa were not observed, and no
evidence exists that appreciable numbers originate from
shallow areas (Lund, 1949). Massive population devel­
opments more commonly originate from exponential
growth of live cells present in the pelagic waters.
Some phytoplankton do settle out during periods
of reduced turbulence and remain in a resting state on
the sediments until water movements are again suffi­
cient to reintroduce the resting cells back into the
plankton. 6 Aulacoseira7 italica is a large diatom that
clearly does enter a resting stage on the sediments,
particularly under ice cover and during summer stratifi­
cation (Lund, 1954, 1955). There is no evidence, how­
ever, for active growth on the sediments, which are
5
Termed boloplankton in older literature, in contrast to meroplank-
ton that have resting stages in sediments and are not observed in the
open water for long periods of time (i.e., they are planktonie only at
certain times in their life history).
6
See page 359.
7
Formerly Melosira.
///. Productivity of Littoral Algae 605
often below the photic zone. Resuspension of filaments
during autumnal and spring circulation serves as a
large inoculum for the rapidly developing pelagic popu­
lation. Similar results have been found for cyanobacte-
ria (Preston et ai, 1980; Fallon and Brock, 1981; cf.
Chap. 15).
In shallow lakes, ponds, and backwater areas of
streams and wetland, the separation between epipelic
or epiphytic algae and littoral metaphyton is less dis­
tinct. It is common to find strictly benthic algae or pre­
dominantly planktonie forms intermixed, especially fol­
lowing irregular storm turbulence (see, e.g., Lehn,
1968; Moss, 1969a; Moss and Abdel Karim, 1969;
Brown and Austin, 1973a). In shallow lakes in which
thermal stratification is irregular and intermittent,
shifts in the percentage composition of largely plank-
tonic or of epipelic algae can be rapid. For example, in
a pond in southern England, nonmotile species domi­
nated planktonie populations only when the water col­
umn was relatively turbulent. Motile species persisted
in the water column, and the largest biomass of any
species occurred when the water column was stratified.
In the shallow Obersee of Lake Constance, southern
Germany, littoral diatoms and algae of the metaphyton
are transported to the open water, especially during
spring storms (Muller, 1967).
III. PRODUCTIVITY OF LITTORAL ALGAE
A. Quantitative Evaluations
Quantitative evaluation of attached algae is basic
to analyses of population changes and productivity but
is confounded seriously by the simultaneous collection
of much debris and dead cells in various stages of
decomposition. Identification, enumeration, and esti­
mation of biovolume, with all proper precautions and
statistical evaluations, have a number of advantages for
detailed analyses (Lund and Tailing, 1957; Lund et ai,
1958; Vollenweider, 1969b; Wetzel and Likens, 1991,
2000; American Public Health Association, 1998). Al­
though developed for plankton, these methods of
analysis usually are equally applicable to studies of
littoral algae. Species enumeration can be used to esti­
mate productivity when coupled to meaningful biomass
parameters such as cell volumes or carbon at the
species level (cf. Chap. 8). Cellular constituents such as
pigment concentrations can be used effectively as an
estimate of attached algal biomass (e.g., Szczepaρski
and Szczepaρska, 1966). It is particularly imperative,
however, to correct for pigment degradation products
(Wetzel and Westlake, 1969; Wetzel and Likens, 2000)
and not to overextend these estimates, which vary
606 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
significantly in response to an array of physiological
conditions.
B. Biomass Measurements
To a limited extent, a temporal series of biomass
measurements permit estimates of rates of primary pro­
duction. These estimates generally underestimate actual
productivity because of losses via excretion of organic
compounds, respiration, mortality, decomposition,
grazing, et cetera. The observed rates also are influ­
enced by the rate of colonization of new propagula,
which is generally faster when conditions for growth
are better. Hence, the observed accumulation of bio-
mass is a composite of colonization and production.
The climax accumulations of biomass on substrata
yield little insight into the production dynamics that
have occurred before the cumulative maximum in bal­
ance between production and losses.
The rate of community turnover is an average of
several variable species rates and is difficult to deter­
mine from biomass analyses. Subjective errors also oc­
cur in determinations of attached algae of lakes and
streams; important factors include the frequency of
sampling and estimation of the degree of colonization
that represents a climax stage of the community
(Slΰdecek and Slΰdeckovΰ, 1964; American Public
Health Association, 1998). Apparently higher turnover
rates result as the sampling interval is decreased, espe­
cially when the intervals are shorter than a month;
sampling frequency must be compatible with reproduc­
tive rates of dominant algal populations.
Productivity values of littoral algae are difficult to
compare from one lake to another, or even seasonally
within a lake, because of the diversity of techniques em­
ployed. Very few in situ metabolic measurements have
been made on these communities. As mentioned earlier,
many analyses have employed artificial substrata to re­
duce the natural heterogeneity of the algae. The resem­
blance of benthic algae on artificial substrates to those
on adjacent natural substances is highly variable and de­
viates significantly, both qualitatively and quantitatively,
with seemingly minor differences in substrata, environ­
mental differences in microhabitats, and particularly in
rates and duration of colonization. The discrepancies
found between populations on natural and artificial sub­
strata are sufficient to necessitate a critical evaluation of
each study in which artificial substrata is used (see, e.g.,
Tippett, 1970; Warren and Davis, 1971). The extent of
compromise must be determined in the application of
any ecological method, and this problem becomes espe­
cially acute among littoral communities.
The admixture of estimates of productivity values
in the ensuing discussion should be viewed as repre­
senting the range encountered under natural condi­
tions. Although no attempt has been made to summa­
rize all of the literature, which is quite diverse and of
variable precision, the examples are presented to point
out primary characteristics and emphasize the major
contributions that the attached flora can make to fresh­
water ecosystems.
C. Spatial and Temporal Variations
The rates of primary production of attached algae
are obviously dependent upon the substrate area avail­
able for colonization within the zone of adequate light.
In some lakes, the littoral substratum may be relatively
uniform for much of the perimeter, but in most cases,
the variation is great. Moreover, living macrophytic
substrata are constantly changing, especially in the
more seasonal temperate regions. An example of this
spatial heterogeneity in productivity can be seen in a 2-
yr analysis of littoral components—macrophytes, lit­
toral phytoplankton, and attached, largely epiphytic,
algae—in Miko³ajskie Lake, northern Poland (Pieczyρ­
ska, 1965, 1968; Kowalczewski, 1965; Pieczyρska and
Szczepaρska, 1966). Simultaneous measurements in
midsummer along numerous points of the littoral zone
showed much variation, which was accentuated during
sporadic mass appearances of sessile cyanobacte-
rium Gloeotrichia and the filamentous green alga
Cladopbora (Fig. 19-17). Similar spatial variations in
numbers and species assemblages have been demon­
strated in the littoral of a eutrophic lake in British
Columbia (Brown and Austin, 1973b).
Seasonal fluctuations in primary productivity of
attached algae are also quite variable, and are analo­
gous to changes in biomass discussed earlier. In general,
estimates of biomass accrual, such as chlorophyll, and
 PERIOD OF AVERAGE GROWTH (JULY 1963)
 PERIOD OF MASSIVE GROWTH (JULY 1964)
—2 —1
X - 1 m g 0 2 dm hr
FIGURE 19-17 Spatial variations in the simultaneously measured
rates of primary production of attached algae in different areas of the
littoral zone of Miko³ajskie Lake, central Poland. (After data of
Pieczyρska and Szczepaρska, 1966.)
 ///. Productivity of Littoral Algae 607

400
0.5 m

z
O
³-
Z
<
_i
CL
O
\-
>
X
CL

J ' F M A M J J A S CD
0
"D
FIGURE 19-18 Rates of primary production of attached algae and
phytoplankton in the littoral zone dominated by the emergent macro­ CM 400
phyte Phragmites. (Modified from Pieczyρska and Szczepaρska, 'E
1966.) o 200
O)
E
0
in situ measurements of production rates by carbon
uptake or oxygen production are fairly similar, particu­ 200
larly during periods of active growth (see Pieczyρska
and Szczepaρska, 1966; Allen, 1971; Hickman, 1971a; 0
Hunding and Hargrave, 1973; Goldsborough and 200
Brown, 1991; Robinson et ai, 1997). Reductions in
temperature and light under winter conditions clearly
are the dominant causal mechanisms limiting photo­ S O N D J F M A M J ' J
synthesis both seasonally and vertically with depth (see FIGURE 19-19 Weekly mean values of gross primary production
Figs. 19-18 and 19-19). The productivity of attached rates of epipelic algae in shallow Marion Lake, a composite from five
littoral stations, southern British Columbia. (Redrawn from Gru-
algae collected under ice and exposed to increased light
endling, 1971.)
was found to increase greatly and approached values
obtained under summer conditions. In the example
from Miko³ajskie Lake, productivity in the spring in­
creased rapidly in both the attached algae and littoral Photosynthetic enhancement of epipelic algae was
phytoplankton, decreased in midsummer during maxi­ shown experimentally when sediment samples were
mum development of the littoral macrophytes, and moved to shallower depths with improved light condi­
then increased in the fall with a bloom of diatoms. tions (Table 19-3). Hunding (1971) has shown that
Where submersed macrophyte biomass persists in benthic diatoms exhibited light-saturated photosynthe­
'evergreen' form under ice, and that ice is not covered sis over a wide range of light intensities. During sum­
by dense light-reducing snow for long periods, attached mer, light-saturated photosynthesis even at very high
algal productivity, particularly by diatoms, can be very irradiances showed no photoinhibition up to 38 klux
high (Fig. 19-15). (= 742 ^tmol quanta m~2 s _1 ). The light-saturated

TABLE 19-3 Enhancement of Photosynthesis of the Epipelic Algal C o m m u n i t y of M a r i o n Lake, British

Columbia, in June by M o v i n g Intact Sediments from Different Depths to 0.5 m*

Solar Incubated in situ Incubated

Sample radiation Temperature at depth at 0.5 m depth
depth (m) {g cal cm~2h~x) (°C) (ml 02 m~ 1h~1) {ml 02 m'1 h-1)

0.5 32.6 23.0 19.9 19.9

1.0 23.3 22.0 22.7 26.4
2.0 14.4 17.0 19.4 28.8
3.0 10.6 14.0 14.5 19.4
4.0 5.5 13.0 2.4 5.7

"From data of Gruendling (1971).

608 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton

TABLE 19-4 Annual M e a n Biomass and Rates of

Primary Production of Epipelic Algae of Abbot's Pond,
Southern England"7
0.5 Y

Mean rate of
Littoral depth Mean biomass (mg primary production
Year category (m) chlorophyll am" 2 ) (mg C m~2 h^1)
E
1966 0-1.0 11.7 5.50
1.0-2.5 7.3 2.89 O
O)
2.5-4.0 4.0 0.56
1967 0-1.0 9.09 4.13
1.0-2.5 1.38 0.75
2.5-4.0 1.47 0.17
1968 0-1.0 13.6 6.23
1.0-2.5 2.14 0.70 A M J J A S O N D J F M A M
2.5-4.0 1.47 0.23 1968 1969
EIGURE 19-20 In situ primary production of attached algae in
*From data of Moss (1969b) and Hickman (1971a)
g C m - 2 of the littoral zone day - 1 among (A) emergent Scirpus acu-
tus, and (B) submersed macrophytes Najas flexilis and Chara,
Lawrence Lake, Michigan. Note marked differences in ordinate
photosynthetic value decreased in autumn, indicating scales. (Modified from Allen, 1971.)
that maximum photosynthetic rates are probably
maintained under reduced prevailing light conditions at
that time of year. Similar depth relationships can be and rates of production of epipsammic algae were con­
seen in comparisons of pigment biomass and primary sistently greater throughout the year than those of
productivity of epipelic algae in a small English lake epipelic algae in the same lake system.
(Table 19-4) and in a clear, deep alpine lake (Cap- Seasonal cycles of primary productivity of epi­
blancq, 1973). phytic algae differ considerably in relation to the type
Within sediments, the rates of carbon fixation and of supporting macrophyte. In the Lawrence Lake
the chlorophyll concentrations of epipelic algae are at­ example shown in Figure 19-20, the annual maxima
tenuated very rapidly with depths of a few millimeters occurred in midsummer when macrophyte biomass,
(Table 19-5), whereas significant rates and pigment and hence substrata for colonization and growth, was
concentrations of epipsammic algae penetrate some­ greatest. At this time conservative estimates exceeded
what deeper. As discussed earlier, the light-mediated 8 g C m - 2 littoral zone day - 1 of carbon fixed by epi­
metabolism of these algae is probably intermittent and phytic algae in this oligotrophic lake. Even though the
occurs predominantly when wave action circulates rates of production per substratum area were similar
sand grains up near to the sediment surface. Biomass among the emergent bulrush Scirpus acutus site and
that of the much more dissected submersed macro­
phytes Najas and Chara, the much greater area avail­
able for colonization in the submersed macrophyte site
TABLE 19-5 Relative Rates of C a r b o n Uptake by Epipelic increased the rates of production by epiphytic algae in
and Epipsammic Algae at Different Depths within Sediment,
the littoral zone area dominated by the two more dis­
Expressed as a Percentage of the M a x i m u m Value, Shear
sected macrophytes. In both cases, annual maxima
Water, England*
were found in August near the sediments at the basal
% of maximum values portions of the macrophytes. Although the winter rates
of carbon fixation by attached algae among the
Epipelic algae Epipsammic algae Najas-Chara were 100-200 times greater than those
among the Scirpus, the values per substrate area among
Dep th (cm) 17 Mar. 68 23 Nov. 67 17 Mar. 68 9 Sept. 68
the more open Scirpus littoral were consistently much
0--1.0 100 100 100 100 higher, ranging from double to an order of magnitude
1.0- -2.0 11.6 57.4 42.1 6.6 higher per area of plant. Causes for this difference are
2.0--3.0 0 33.4 5.7 0.2 unknown, but the more open Scirpus bed had greater
3.0--4.0 0 30.5 3.1 1.2 light and water movement than occurred in the dense
4.0--5.0 0 14.3 2.5 0.3
Chara beds. Furthermore, as discussed in Chapter 18,
^ All samples incubated at the same light conditions. From data of the macroalga Chara is known to release sulfur-
Hickman and Round (1970). containing organic compounds that are antimicrobial.
TABLE 19-6 Rate of Production of Attached Algae and Estimated Turnover Rates of the Algal Populations of Several Exemplary Aquatic Systems

Average annual
Average estimated net Estimated
biomass productivity turnover time
Lake Type of algae (g dry m~2) [mg dry m~2 day'1) {days) Source

Sodon Lake, MI
Falls Lake, WA
Alkali Lake, WA
Sedlice Reservoir,
Czechoslovakia
Lake Glubokoye, Russia
Silver Springs, FL
Laboratory analyses,
diatoms of Lake
Balaton, Hungary
Jeziorak and Tynwald,
northern Poland
Raspberry Pond, Manitoba
Crescent Pond, Manitoba
Suomunjΰrvi, Finland
Pΰΰjΰrvi, Finland
Changing, Antarctica
Sombre, Antarctica
Tundra, Ponds, Alaska
Tamagawa River, Japan
Glass slides, horizontal, 1.23 37.5 32.8 Newcombe (1950)
open water
Glass slides, horizontal, at 3.24 148 21.8 Castenholz (1960)
sediment interface (0.4 m)
Glass slides, horizontal, at 2.94 131 22.4 Castenholz (1960)
sediment interface (0.4 m)
Glass slides, vertical, open water, 12.7 213 59.6 Sladeζek and Slΰdeckovΰ (1963)
several depths
Epiphytic on Equisetum, biomass, 18.7 128.8 21.7 Assman (1953)
and 0 2 production
Epiphytic on Sagittaria, biomass, 177 12,300 14.4 Odum (1957)
and 0 2 production
Epilithic diatoms, biomass, and — — Approx. 1 (optimal Felfoldy(1961)
0 2 production conditions)
Glass slides; in reed zones — — 4.5-16 Bohr and Luscinska (1975)
Epiphytic on rods in dystrophic — 1700 — Goldsborough and Brown (1991)
pond; 14C methods
Epiphytic algae on macrophytes; 40 147 — Hooper and Robinson (1976, 1978)
14
C methods
Epipelic algae of an oligotrophic — 1.1 — Sarsa (1979)
lake; 14C methods
Epipelic algae, 14C methods — 60 — Kairesalo (1976, 1977)
Epipelic algae, 14C methods 6
Epipelic algae on rocky debris; — 18 — Priddle (1980)
0 2 methods
Epipelic algae on rocky debris; — 49 — Priddle (1980)
0 2 methods
Epipelic algae of shallow ponds; — 22-55 — Stanley (1976)
14
C methods
Glass slides Aizaki (1979)
Bacteria — — 0.13-0.42
Algae — — 0.5-1.2
610 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton

In an oligotrophic lake in New York, photosyn-
thetic rates of epiphytic algae were approximately 5%
of the photosynthetic rates of the supporting macro-
phytes (Sheldon and Boylen, 1975). Epiphytic algal
densities increased with the seasonal growth patterns of
the macrophytes; maximal algal colonization of leaves
of the plants, however, was similar per unit time. Epi­
phytic algal productivity from older leaves, lower on
the macrophyte, was as much as 10-fold greater than
that of epiphytes from younger top leaves. Similar
results were found in the more detailed studies of
Burkholder and Wetzel (1989a).
Rates of epiphytic bacterial utilization of simple
organic substrates (glucose and acetate) followed first-
order active transport kinetics (Allen, 1971). These
rates were nearly an order of magnitude greater per
unit area in the submersed macrophyte littoral region
than among the emergent plants. This difference is
potentially related to the greater quantities of organic
substrates released by the submersed plants than by
emergent macrophytes.
A comparison of production rates of attached
algae among lakes and climatic regimes is difficult be­
cause of the variety of methods that have been used.
However, there is a clear tendency for the rates of
primary productivity of the attached algae to increase
with decreasing latitude and longer growing season
(Tables 19-6 and 19-7). The turnover times of the
attached algal populations also tend, not unexpectedly,
to decrease under the better growing conditions. The
highest production values recorded are from sub­
tropical springs in which constant temperatures, high
flow, and adequate nutrient supplies combine to en­
hance high rates of production. A similar relationship
is seen among streams (cf. Wetzel, 1975b; Aizaki,
1978; Wetzel and Ward, 1992), although available data
are few and very difficult to compare in a satisfactory
manner.
A comparison of the rates of in-stream primary
productivity of attached algae among intensively stud­
ied sites from many geographical and geological re­
gions of North America showed rates to be similar
(Table 19-8). Concentrations of chlorophyll a of ben-
thic microbiota spanned an order of magnitude
(10-100 mg m~2) with little geographical differentia­
tion within a seasonal range of ca. 1-300 mg m~2.
Highest amounts were found in open plains or desert
regions of high productivity.
Gross primary productivity of within-stream ben-
thic algae (Table 19-9), as well as community respira­
tion (e.g., consumption of dissolved oxygen in 24 h),
commonly increases with downstream direction (e.g.,

TABLE 19-7 Comparisons of N e t Rates of Production of Attached Algae, Expressed as Organic M a t t e r Accrual over a 10-Day
Period, of Several Different Fresh Waters*

Depth of maximal
Mean net production rate net production
Lake (mg org. mat. dm~2 day'1) accrual Remarks

Sodon Lake, MI 0.5 0.2 m Horizontal glass slides, 3 summer months;

Newcombe(1950)
Falls Lake, WA 1.28 0.4 m Horizontal glass slides, 22 months;
Castenholz(1960)
Lenore Lake, WA 1.00 0.4 m 17 months
Alkali Lake, WA 1.76 0.4 m 12 months
Soap Lake, WA 1.67 0.4 m 17 months
Walnut Lake, MI 1.69 0.6 m Horizontal glass slides, 2 summer months;
Newcombe (1950)
Sedlice Reservoir, 2.13 3.0 m Vertical slides, 10 months; Slΰdecek and
Czechoslovakia Slΰdeckovΰ(1964)
Lake Tiberias, Israel 2.20 1.2 m Vertical glass slides, 14 months; Dor (1970)
Shallow ponds, central MI 3.63 Glass slides, 2 summer months; Knight
et al. (1962)
Borax Lake, CA 14.63 14
C methods, 12 months, in situ on
0.2 m
epilithic algae; Wetzel (1964)
Red Cedar River, central MI 21.2 Plexiglas plates, summer months; King
and Ball (1966)
Tiberias Hot Springs, Israel 73.0 Horizontal glass slides, 2 months; Dor (1970)
0.1 m
Silver Springs, FL 96.7 0 2 methods, epiphytic on Sagittaria,
12 months; Odum (1957)

Techniques employed vary widely and only an approximate comparison is possible.

 ///. Productivity of Littoral Algae 611

TABLE 19-8 M e a n Annual N e t Primary Productivity of In-Stream C o m m u n i t y

Producers of N o r t h American Streams

Mean annual net community

primary productivity
(mg carbon m~2 day'1)

Eastern deciduous forest stream, coastal - 2 7 . 0 - 2 4 6 . 8 (* 4 127.4)

climate, Pennsylvania*
Mesic hardwood forest stream, continental - 5 5 . 9 - 4 8 6 . 4 {x4 207.3)
climate, Michigan*
Cool, arid climate stream, much precipitation as 48.2-524.7 (3c7 415.2)
snowfall, coniferous vegetation on north-facing
slopes, sagebrush on south-facing slopes, Idaho*
Northern cool-desert stream open, no canopy, Idahofe
Autochthonous
Macrophytes 47.2-147.6 (5t3 93.4)
Periphyton 465.6-1748.0 ( * 3 1004)
Allochthonous particulate organic matter 0.7-16.9 (x3 7.0)
Coniferous forest stream, coastal climate, Oregon* - 2 1 . 0 - 9 3 . 8 (x4 45.1)

* Extracted from data of Bott (1983).

Calculated from Minshall (1978) assuming 1 kcal = 4.6 g organic matter and 46.5% carbon
in organic matter of aquatic plants (Westlake, 1965).

TABLE 19-9 Examples of Rates of In-Stream Primary Production of Benthic Algae

Mean primary productivity

Site [mg carbon m~2 day'1) Technique Source

Direct estimates:
Morgans Creek, KY 0.7-4 Biomass change Minshall (1967)
Walker Branch, TN 8-11 Biomass change Elwood and Nelson (1972)
14C
Glade Branch, VA 10 Uovmcketal (1981)
Piney Branch, VA 11 14C
Hornickζtfa/. (1981)
14C
Guys Run, VA 18 Wormcketal. (1981)
Berry Creek, OR 99 Oxygen exchange in Reese (1967)
recirculating chamber
Yellow Creek, AL 49.3 14C
Lay and Ward (1987)
Little Schultz Creek, AL 91.2 14C
Lay and Ward (1987)
Amazon River, Brazil 465-1040 14 C Putz (1997)
Whole community estimates:
New Hope Creek, NC* 330-1430 Diurnal oxygen curve Hall (1972)
Riera Major, Spain 137 Diurnal oxygen,
metabolism chamber Guasch and Sabater (1998)
La Solana, Spain 430 Diurnal oxygen, metabolism Guasch and Sabater (1998)
chamber
Ober Water, England 103 Biomass change and estimated Shamsudin and Sleigh (1994)
generation times
River Itchen, England 822 Biomass change and estimated Shamsudin and Sleigh (1994)
generation times
Deep Creek, ID 1180 Oxygen exchange, Minshall (1978)
upstream / downstream
Catahoula Creek, MS 1850 Oxygen exchange, de la Cruz and Post (1977)
upstream / downstream
White Clay Creek, PA 2220 0 2 / C 0 2 exchange Bott et al (1978)
a
Enriched by fertilizer and sewage.
612 W. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
Bott et al, 1985). Photosynthetic efficiencies of benthic
algae are generally below 4 % , with averages near 1%,
and decline downstream with increasing light availabil­
ity (Fig. 15-20).
D. Production Rates of Attached Algae versus
Phytoplankton and Macrophytes
Few detailed studies exist in which in situ measure­
ments of productivity of attached algae, phytoplank­
ton, and macrophytes have been made simultaneously
(Table 19-10). However, these studies are important in
that they demonstrate the magnitude of effect that lit­
toral productivity can have on lake systems. The range
is great. In the large, shallow Borax Lake in northern
California, epilithic algae are a major source of organic
matter. Because the littoral area is small, when produc­
tivity per unit area is expanded for the whole lake sur­
face, the attached algal contribution is reduced but still
constitutes nearly one-half of total primary productiv­
ity. In Marion Lake, the primarily epipelic algae domi­
nate the lake system. In Lake Wingra, Wisconsin, the
submersed macrophytes are major components of the
total primary productivity. Littoral attached algae,
largely epiphytic, of Lawrence Lake constitute nearly
three-fourths of the primary lake productivity, in spite
of the limited littoral area of this small, moderately
deep lake (Table 19-10). In contrast, the littoral contri­
bution to the total productivity of the two Ontario
lakes constitutes only a few percent because the mor-
phometry and geology of these lakes do not lend them­
selves to extensive littoral development.
A few other, less complete studies that do not per­
mit full comparisons should be mentioned to relate the
relative rates of photosynthesis of attached algae to
those of phytoplankton. Slow-growing submerged
mosses, almost exclusively Marsupella aquatica, cover
some 40% of the bottom from between 2 to 35 m of
clear, low mountain Lake Latnajaure in Swedish Lap­
land (latitude 68°). This large, deep (z = 16.5 m, zm =
43.5 m) lake is covered with over a meter of ice for
about 10 months of the year and has a mean annual
water temperature of 2°C. During the period of investi­
gation in August and September, the average primary
productivity for the whole lake was between 3.5 and
4.0 kg C per day (Bodin and Nauwerck, 1969). The
average turnover time of the biomass of the perennial
moss was about 30 y, between extremes of about 15 y
at a depth of 5 m and 125 y at depths greater than
30 m. Of the total primary productivity of the lake, the
phytoplankton were responsible for 60%, the moss for
20%, the epipelic diatoms for 15%, and the epiphytic
algae on the moss for 5%. Similar results have been
found in Char Lake in the Canadian Arctic at latitude
75° N (Kalff and Wetzel, unpublished).
Evaluation of the productivity of phytoplankton
and attached algae of a large, deep alpine lake of the
central Pyrenees Range also indicated the major contri­
bution of the macroalga Nitella and of epilithic algae
to the total primary productivity (Capblancq, 1973).
The attached algae of the littoral zone ( 0 - 6 m) and
Nitella (6-19 m) formed a biomass some 140 times
greater than the mean biomass of the phytoplankton
during summer, and Nitella constituted about 80% of
the total benthic algae. Based on in situ productivity
measurements, the contribution of benthic algae to the
total primary productivity of this lake was estimated to
be 30%.
The work of Straœkraba (1963) on two large, shal­
low fishponds of southern Czechoslovakia deserves par­
ticular mention. Based on extensive annual cycles of the
nitrogen content and biomass dynamics of all plant and
animal components of these shallow lakes, it was deter­
mined that about 7 3 % of the primary productivity re­
sulted from largely emergent macrophytes, 20% from
attached, mainly epiphytic algae, and 7% from phyto­
plankton. It was shown that < 1 0 % of the primary pro­
ductivity was utilized by higher trophic levels.
Studies evaluating the relative photosynthetic rates
of algae of the littoral in comparison to the rates of
phytoplankton are few. But the suggestion that the
most productive site is epiphytic on macrophytes re­
peatedly appears, as shown, for example, Table 19-11
for a shallow English lake, Lawrence Lake, discussed
earlier (Table 19-10), and in the littoral of Miko³ajskie
Lake (Table 19-12). Among the most detailed and in­
structive studies of the relative contributions of the at­
tached algae of different substrata is from long-term
analyses of periphyton of the extensive wetland on the
shores of Lake Manitoba (Robinson et al., 1997).
Epiphytic and particularly metaphytic algae totally
dominated the littoral algal productivity (Table 19-13),
and production rates declined markedly as mean water
levels were raised by half a meter.
These results support earlier discussion on the im­
portance of factors of light, which is often coupled to
water levels in shallow areas, wave action-sediment
movement, and inorganic-organic nutrient exchanges
between macrophytes and attached algae. It is apparent
that growth conditions are often better in the littoral
attached habitat than in the planktonie habitat. The
significance of littoral productivity to a lake system de­
pends to a great extent on the physical conditions of
the lake morphometry, light availability, and character­
istics of the substrata available for algal attachment
and growth.
TABLE 19-10 Examples of Annual Net Productivity of Phytoplankton, Littoral Algae, and Macrophytes of Several lakes in Which Productivity Estimates of Attached Algae
Were Made on Natural Substrata

Area Mean Annual mean Annual mean kg C ha-1 of lake

Lake (ha) depth (m) (mg Cm~2 day'1) (kg C lake'1 day'1) surface yf - i Remarks

Borax, CA 39.8 <0.5 (%) Saline lake; benthic algae,

Phytoplankton 249.3 101.0 926 (56.8) primarily epilithic, some
Littoral algae 731.5 75.5 692 (42.5) epiphytic and metaphyton;
Macrophytes 76.5 1.36 12 (0.7) single macrophyte species
Ruppia maritima;14C methods
1630 for all components (Wetzel, 1964)
Marion, British Columbia 13.3 2.2 Softwater, oligotrophic lake;
Phytoplankton 21.9 0.29 8 (1.6) benthic algae, primarily epipelic;
Littoral algae 109.6 11.3 310 (62.2) 0 2 techniques, from which net
Macrophytes 49.3 6.5 180 (36.1) production was estimated
(Efford, 1967; Hargrave,
498 1969; Gruendling, 1971)
Lake 239, Ontario 56.1 10.5 Softwater, oligotrophic lake;
Phytoplankton 823 (99.0) probably underestimates
Littoral algae 8.1 (LO) since winter production is
Macrophytes N.D. not included; benthic algae,
primarily epilithic, macrophytes
ca. 831 probably insignificant; C 0 2
utilization methods
(Schindler e* a/., 1973)
Lake 240, Ontario 44.1 6.1 (Same as for Lake 239)
Phytoplankton 501 (98.2)
Littoral algae 9.0 (1.8)
Macrophytes N.D.
ca. 510
Lawrence, MI 5.0 5.9 Hardwater, oligotrophic marl lake;
Phytoplankton 118.9 5.90 430.8 (13.2) benthic algae are primarily
Littoral algae (<1 m) 2001 15.10 1102.4 (33.7) epiphytic on sparse submersed
Littoral algae ( 1 - 5 m) 500 16.35 1193.6 (36.6) macrophytes; 14C methods
Macrophytes 240.8 7.40 540.2 (16.5) (Wetzel et al, 1972, and
44.75 3267.0 100.0 refinements of analyses of epiphytic
algae in Burkholder and
Wetzel, 1983b)

(continues)
 TABLE 19-10 (Continued)

Area Mean Annual mean Annual mean kg Cha 1 of lake

Lake (ha) depth (m) (mg C m - 2 day-1) (kg C lake~ 1 day~x) surface yr~l Remarks

Wingra, WI 139.6 ca. 2 (%) Large, shallow, hardwater eutrophic

Phytoplankton 1200 1675 4380 (78.6) lake; large littoral zone with
Metaphyton (Summer, 1971) 3.0 4.2 11. (0.4) dominant submersed macrophyte
(Oedogonium) (Summer, 1972) 5.5 7.6 19.9 Myriophyllum and metaphytic
Macrophytes 320.5 447 1170 (21.0) mats of macroalga Oedogonium;
14
5581 C methods for all components;
mostly only summer values
(McCracken et al, 1974; Adams
and McCracken, 1974; J. F. Koonce,
personal communication)
Neusiedlersee, Austria 30,000 1.3 Large, shallow, 66% in Phragmites
Phytoplankton (open lake) 235 stands; various methods, mostly
Phytoplankton (littoral) 20 annual values (Khondker and
Epiphytic algae 11.6 Dokulil, 1988)
Epipelic algae 50
Emergent Phragmites 2740
Submersed macrophytes 254
Algal, Antarctica — <0.5 Shallow oligotrophic lake;
Epipelic algae 468 dense epipelic algal mats; 14C
Phytoplankton techniques (Goldman et al., 1972)
Kalgaard, Denmark 10.5 4.7 Small oligotrophic, softwater lake;
Phytoplankton 14
241 (52.3) C techniques for phytoplankton
Littoral algae 5 (1.1) and epiphytes; biomass of
Macrophytes 215 (46.6) macrophytes (Sondergaard and
Sand-Jensen, 1978)
Watts, Antarctica 38 ca. 5 Shallow, oligotrophic, continental
Epipelic algae 15.1 lake; 14C techniques (Heath, 1988)
Phytoplankton 27.7
Laca, Russia 16,600 Large, shallow, eutrophic
Phytoplankton 996 (36.9) lake; macrophytes colonizing
Littoral algae 725 (26.9) 48% of lake area; biomass
Macrophytes 979 (36.3) methods (Raspopov, 1979)
Eagle, CA 12,150 7.0 Large, subalpine, hardwater,
Phytoplankton 356 50,860 168 (85.8) eutrophic lake; oxygen and
Epilithic algae 274 3800 95 (7.0) biomass techniques (Hunt-
Epiphytic algae 1153 1919 47 (3.5) singer and Maslin, 1976)
Macrophytes (emergent) 1249 2690 51 (3.8)

TABLE 19-11 Mean Rates of Primary Production of Phytoplankton in Relation to Those of
Epipelic Algae and Algae Epiphytic on the Horsetail (Equisetum fluviatile L.)
Lake
Eutrophic, shallow; Priddy
Pool, England*
Oligotrophic, deep, with limited
littoral area; Lake Paajarvi, Finland*7
0-1 m
2-4 m
a
Mean annual values; based on data of Hickman (1971b).
Mean summer values; Kairesalo (1980b).
E. Changing Littoral Productivity and Eutrophication
As lakes receive increasingly large loads of nutri­
ents per unit volume per time, there is a strong ten­
dency for phytoplankton to increase to the m a x i m u m
capacity within existing limitations of temperature and
available light (cf. C h a p . 15). However, it is imperative
that eutrophication of aquatic systems is not viewed in
the restricted sense of phytoplanktonic productivity.
Within obvious geomorphological restrictions on wet­
land and littoral development at the l a n d - w a t e r inter­
face regions, the c o m m o n situation is for littoral pro­
ductivity to play a major role in early and in final
stages of increasing fertility of the lake system as a
whole. Exceptions certainly exist, but these conditions
of major littoral production are clearly widespread be­
cause a large percentage of lakes of the world are small
in area and shallow.
A c o m m o n natural or human-induced disturbance
to lake and reservoir ecosystems involves progressive
TABLE 19-12 Percentage Contribution of Various Producers
to the Annual Net Primary Productivity per m 2 in the Littoral
Zone, Miko³ajskie Lake, Poland*
Zone / component
Eulittoral
Macrophytes
Planktonie
Metaphyton
Attached algae
Littoral overgrown with emergent vegetation
Macrophytes
Planktonie
Metaphyton
Attached algae
* After Pieczyρska (1970).
///. Productivity of Littoral Algae 615
Epiphytic algae
Phytoplankton Epipelic algae (mg C m~2 of
(mg C m~2 h~l) (mg C m~2 h~x) substratum h~l)
1.55 1.71 63.9
5.35 3.68 3.6
3.85 1.68 —
increases in loading of nutrients. These loadings, in ex­
cess of losses to sites of temporary or permanent inacti-
vation such as sediments, result in enhanced nutrient
availability for phytoplankton and other autotrophs
with increased rates of growth and productivity. If nu­
trient loadings increase to an oligotrophic lake, in­
creased productivity is rapid. Similarly, if the distur­
bance is brief (i.e., the duration of increased nutrient
loading is relatively short), nutrient cycling is rapid, the
ecosystem will recover rapidly, and productivity will be
reduced proportionally to the load reduction.
As nutrient loading increases, particularly among
shallow lakes that predominate globally (Wetzel,
1990), a m a r k e d shift in the productivity occurs from
the pelagic to attached surfaces associated with living
aquatic plants and the particulate detritus of senescing
macrophyte biomass (Fig. 19-21). Under these condi­
tions, the primary productivity and biomass of the
lake ecosystem increase greatly. H a b i t a t diversity
a m o n g the massively dissected surfaces of submersed
aquatic plants and particulate detritus of the sediments
increase exponentially. As nutrient loading increases
further, phytoplanktonic productivity per unit volume
increases, but self-shading by the algae restricts the
depth of the trophogenic zone. Within a given latitude
Percentage
and climate, m a x i m u m growth of phytoplankton in
contribution
fertile waters is determined by light reduction induced
by self-shading; g r o w t h can be increased beyond these
28 limits only by increasing turbulence and light avail­
10 ability to levels greater t h a n those normally found un­
21
der natural conditions (Wetzel, 1966b). Phytoplank­
41
tonic productivity per unit area declines precipitously
57.2 under these eutrophic conditions and is usually accom­
19.6 panied by a m a r k e d decrease in planktonie biodiver­
0.1 sity as well.
23.1
This light limitation, usually associated with in­
tense phytoplanktonic and epiphytic algal productivity,
616 19. Land- Water interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton

TABLE 19-13 Comparison of Primary Productivity of Attached and Planktonie Algae of a Wetland of Manitoba
under Different Water-Level Regimes*

Mean daily productivity

(mgC m 2 wetland area)

Mean algal biomass Low Medium High Percentage

(mg chi. a m 2 water water water contribution (mean
wetland area) level level level all water levels)

Phytoplankton 7 169 209 225 7.3

Epipelic 4 32 47 15 1.0
Epiphytic 67 1003 813 353 22.2
Metaphyton 530 2863 2372 1338 69.5
Total m~2 4067 3441 1931 100.0
:
^Ice-free period (5-6 months); mean of five years. Low water = 7-28-cm depth; medium water = 37-58-cm depth; high water
67-88-cm depth. Extracted from data in Robinson et al. (1997).

thus extends to submersed aquatic plants. Light attenu­
ation is critical. Dense phytoplankton populations
alone are sufficient to attenuate light to a point where
it is inadequate to support growth of submersed
macrophytes (e.g., Mulligan et ai, 1976; Jupp and
Spence, 1977). Reductions in phytoplankton densities
and improved light conditions (e.g., by reductions in
nutrient or turbidity loading or by selective fish preda-
tion on zooplankton, which in turn alters phytoplank­
ton composition; Chaps. 15 and 16; Leah et al., 1980)
can result in recolonization by submersed macrophytes.
In addition, increased nutrient loading can increase epi­
phytic growth on macrophytes to the point of severely
reducing the amount of light reaching the supporting

>* Nutrient Submersed Light ,'~

 > Limitations Limitations /«.Emergent

T3
13 ³ 1

/
/
/ Macrophytes

O /
u- /
a.
>» * ^N
i*_
0*
s'* 1 \
1 \
E Submersed !
Macrophytes / \
CL /  j ^ - ^ j Epiphytic Algae
S^ s ^ i \ ! , and Metaphyton
>
<D
/ v y \\ t-—
yy
-*—» / S «" \ \ /
-23 ^^^^ V Phytoplankton
CD
r
DC
**6^ ' '" x ^ j
Low High
Gradient of Nutrient Loading
to Shallow Lakes
FIGURE 19-21 Relative changes in primary productivity of phytoplankton, macrophytes,
and attached microflora along a gradient of nutrient loading to a spectrum of lake ecosys­
tems. (From Wetzel, 1999a, expanded and modified from Wetzel and Hough, 1973.)
 IV. Periphyton among Aquatic Ecosystems 617

macrophytes (e.g., Sand-Jensen, 1977; Phillips et al, 10*

1978; Tsuchiya and Iwaka, 1979; Sand-Jensen and
S0ndergaard, 1981).
10'
Submersed light limitation thus can reduce or elim­
inate submersed macrophyte growth and much of
the attendant surfaces for microbial growth. The elimi­ icr
nation of attached algal photosynthesis by attached
microbiota decouples the metabolic mutualism to the
attached heterotrophs and decreases collective produc­ a> io
tivity markedly (Wetzel, 1993a; Neely and Wetzel,
1995). The losses of attached microbial communities 2 io*
and their coupled metabolism cause a massive reduc­ u. (Littoral
tion in the capacities of the land-water interface re­ O Only)
cr io
gions of freshwater ecosystems to retain loaded nutri­ UJ
ents and dissolved organic compounds. CD

Continual high nutrient loading and hypereu- 1.0' P/W + L

trophic phytoplanktonic conditions generate large ar­ [Littoral +

eas of anaerobic reducing conditions and lower rates of
decomposition of organic matter. Production exceeding
decomposition leads to rapid sedimentation and the
generation of increased shallow habitat conducive to
colonization by emergent macrophytes (Fig. 19-21).
The high productivity of emergent macrophytes in­
creases the proportion of lignocellulose supporting tis­
sues that are relatively recalcitrant to rapid decomposi­
tion, particularly under reducing conditions (Wetzel,
1979).
As the emergent vegetation assumes greater domi­
nance in a lake ecosystem, and eventually covers a
majority of the lake basin (see Chap. 24), an exceed­
ingly productive combination of littoral macrophytes
and attendant microflora develops. Attached, largely
epiphytic algae, eulittoral algae, and metaphyton de­
velop in association with the emergent flora. Natural
changes in this general sequence are usually slow and
may extend over centuries and millennia, depending
on the basin morphometry. The process can be accel­
erated greatly by increased nutrient loading, either ar­
tificially (e.g., Hasler, 1947; Smith, 1969) or more
gradually (e.g., Mattern, 1970). The collective result
is markedly increased total ecosystem productivity,
largely because of the high emergent macrophyte
production.
The ratio of the interface zones to the pelagic per­
mits one to estimate the importance of the littoral in re­
lation to the pelagic zone. Most of the lakes of the
world are small, and their morphometry is such that
the ratio of the pelagic zone (P) to the colonizable lit­
toral zone (L) is small (Fig. 19-22). On a global basis,
the littoral zone is clearly dominant over the pelagic
(low P/L ratios) among most standing-water and river
ecosystems. Addition of the wetland components to the
littoral zone results in low ratios (P/W + L) for nearly
Wetlands)
10
0.01 0.1 1 10 100 1000
PELAGIC/LITTORAL RATIO
LITTORAL PELAGIC
DOMINATED DOMINATED
FIGURE 19-22 Number of lakes of the world in relation to the ra­
tios of pelagic to littoral and wetland regions. (From Wetzel, 1990a.)
all standing-water ecosystems (Fig. 19-22). In these
cases, there is little question that production of macro-
phytic vegetation, and importantly, its attendant mi­
crofiorai community, has major impacts on the lake
ecosystem.
The distinction between what constitutes al-
lochthonous production (e.g., eulittoral, terrestrial, et
cetera) and what is part of true autochthonous lake
production is an extremely artificial one and has, in­
deed, led to an artificial treatment of mechanisms con­
tributing to and influencing ecosystem metabolism. All
components of the drainage basin are influential in reg­
ulating lake metabolism. Integrated data on the func­
tional impact of these components on the entire system
are essentially nonexistent. The concept of a lake as a
microcosm must finally be laid to rest.
IV. PERIPHYTON AMONG AQUATIC ECOSYSTEMS
Comparison of the periphyton communities and
their productivity among river, reservoir, lake, and wet­
land/littoral ecosystems is difficult because of the high
TABLE 19-14 Comparative Characteristics among Periphyton Communities of River, Reservoir, and N a t u r a l Lake Ecosystems and Wetland Interface Regions

Characteristic Rivers Reservoirs Natural lakes Wetland/littoral areas

Periphytic algal
diversity
Periphytic algal biomass
and production
Herbivory pressures on
periphyton
Attached/littoral
"zooplankton"
Low in-channel, moderate
in floodplain wetlands
and backwater areas
Low in-channel, especially
in low-order, canopied
streams; increasing among
mid-order (3-5) streams;
low in large rivers; moderate
to high in floodplain wetlands
and backwaters
Moderate to high seasonally
in middle-order streams
Low, restricted to floodplain
and backwater areas; dominated
by r-selected species that are
adapted to frequent disturbances
Low, often restricted by severe
water-level fluctuations and
turbidity; macrophyte habitat
often very low
Low, often restricted by limited
substrata in photic zones and
low submersed macrophytes
Low, restricted availability
Very low, restricted stable
habitat and macrophytic refuges
Low in epilithic, moderate
in epipelic, and very high
in epiphytic communities
High on two-dimensional
surfaces (sediments, rocks)
to very high on three-
dimensional substrata
(submersed plants)
Low to moderate, distinctly
seasonal; largely a
production-detrital system
dominated by microbial
heterotrophy
High, large-sized among macrophyte
habitats offering predation refuges
and abundant food
Very high among great habitat diversity
of living and dead vegetation and
particulate detritus
Very high on abundant livingand detrital
surfaces among shallow waters
Low, largely a production-detrital system
dominated by microbial heterotrophy
Nearly all sessile, attached forms;
predation relatively low in comparison
to more open lake littoral regions

variability among habitats and their dynamic nature.
Attached algal diversity is relatively low within the
high-velocity portions of river channels but is consider­
ably greater among the greater, somewhat more stable
floodplain and backwater areas (Table 19-14). The
high and variable turbidity and water-level fluctuations
in many reservoirs preclude the development of moder­
ately stable and diverse substrate habitat. In contrast,
habitat diversity and attached algal diversity is ex­
tremely high among the littoral areas, particularly
among submersed macrophytes and in wetland areas of
abundant particulate detritus.
Attached algal and cyanobacterial productivity
and biomass development is moderately high in mid-
order (3-5) streams and in backwater areas but low
in light-restricted, canopied low-order streams and in
more turbid large rivers (Table 19-14). The productivity
of phytoplankton, periphyton, and macrophytes be­
comes much more complicated in the highly dynamic
large rivers of the tropics, such as the Amazon and
Paranΰ/Paraguary river ecosystems. During the seasonal
flood pulse, large fluctuations occur in periphyton de­
velopment and productivity in relation to currents
within backwater pools and ponds, loss of vegetation
and associated substrata, and turbidity imported with
the river water (Nieff, 1990; Junk, 1997). Limited habi­
tat, substrata, and light often preclude extensive at­
tached algal developments in reservoir ecosystems. Pro­
ductivity and high biomass turnover occur in littoral
and wetland areas, particularly among the high surface
areas in well-lighted regions of submersed macrophytes
and particulate detrital masses.
Herbivory by immature aquatic insects, other inver­
tebrates, and certain fish can impose significant mortal­
ity on periphyton communities of streams at certain
times of the year. In standing waters, production by pe­
riphyton is often greater, and herbivory is appreciably
less than in many streams. In many productive littoral
and wetland areas, the periphyton community is largely
a production-detrital system dominated by microbial
utilization of the attached autotrophic production.
V. LITTORAL ZOOPLANKTON COMMUNITIES
Littoral zooplankton communities are made up of
a diverse assemblage of protozoans and other protists,
rotifers, and microcrustaceans. Many of these animals
are sessile upon the sediments or macrophytes and are
not truly planktonie, or are only intermittently plank-
tonic. The number of species within littoral macro-
phyte zones is generally larger among all groups of or­
ganisms than in the open-water zone of lakes, ponds,
or rivers (e.g., Pennak, 1966).
V. Littoral Zooplankton Communities 619
Littoral zooplankton have been studied much less
intensively than have pelagic forms. Many of the life
history, reproductive, and population characteristics of
pelagic zooplankton, discussed at length in Chapter 16,
are equally applicable to littoral-inhabiting zooplank­
ton. A few conspicuous characteristics of the littoral
fauna are noteworthy.
Microcrustacean communities have been found
to fall into three general groups in the littoral zone:
(a) highly "plant-associated" and infrequently found
away from aquatic macrophytes, (b) "free-swimming"
among the large plants, and (c) sessile and living
mainly in littoral sediments (e.g., Pennak, 1966; White-
side et al, 1978, Fairchild, 1981). Truly planktonie
species are common in areas within littoral zones de­
void of vegetation but are rare within areas densely col­
onized by macrophytes. Among the large plants, free
zooplankton are predominantly plant browsers or sedi­
ment-inhabiting species that are temporarily swimming
or open-water species that enter vegetated areas and
develop under conditions of reduced predation pres­
sures from fish.
Plant-associated microcrustacean taxa are often
closely associated with macrophyte species or morpho­
logically similar plant types (Quade, 1969, 1971) and
are distributed according to available surface area
(Fairchild, 1981). Numbers of Cladocera feeding on de­
trital periphyton were significantly correlated with epi­
phytic diatom density, whereas filter-feeding Cladocera
attached to the plants were not. Similar animal-plant
associations have been found among littoral rotifers
(Edmondson, 1944, 1945; Wallace, 1978). Few benthic
or epiphytic microcrustacea enter the water column,
even at night (Paterson, 1993).
Among the common littoral microcrustaceans are
the chydorids; most chydorid species increase in num­
bers during spring and autumn and decrease during
midsummer (Goulden, 1971; Keen, 1973; Whiteside,
1974, 1988; Vuille, 1991). In a detailed study of the
population dynamics of four species of a hardwater
lake in southern Michigan (Keen, 1973), for example,
Chydorus sphaericus reached its maximum population
density in the spring, declined to a low level in the
summer, and then increased to a smaller fall peak pre­
ceding a winter plateau (Fig. 19-23). It is common for
Chydorus to become abundant in the open water in
summer, coincident with the minimal littoral popula­
tions. As indicated in the upper portion of the figure,
production of males and ephippial females was very
small in this littorally perennial species. In contrast,
Graptoleberis, Acroperus, and Camptocerus are aesti-
val and after a winter absence appeared in spring, from
ephippial eggs, and attained maximal densities in late
summer and autumn (Fig. 19-23). The latter maxima
620 19. Land- Wa ter In terfaces: A ttached Microorganisms, Littorai Algae, and Zooplankton

2500

A S I O 'N A SIO N
1969 1968 I9fi9 196ft
FIGURE 19-23 Annual population densities of the four major species of littoral chydorid cladocerans
among submersed beds of Scirpus subterminalis, west littoral, Lawrence Lake, Michigan. Upper panels
show percentage of the population of Chydorus and Acroperus seasonally in juveniles, females, females
with eggs, males, and ephippial females. (Redrawn from Keen, 1973.)

terminated with the massive development of ephippial
females and males prior to winter. Natural death and
emigration were not clear but assumed to be negligible
in this and several similar studies. High summer
mortality was associated with active predation by small
fishes (<4 cm in length) and nymphs of dragonflies
(Odonata). In another analysis (Goulden, 1971), the
midsummer population minima of chydorids were
largely caused by predaceous tanypodine midge larvae.
The midges were rare or absent in spring and autumn
when the chydorids were most abundant.
In contrast, temporal and spatial correlations of
distribution patterns of chironomid larvae of littoral
sediments and chydorid cladocerans in the sandy lit­
toral areas of a mesotrophic lake were very weak (van
de Bund et al, 1995). Alterations in species abun­
dances need not always be associated with predation,
however. For example, positively phototactic swarming
of the cladoceran Bosmina and movement of large por­
tions of the populations from littoral areas to the
pelagic zone have been documented (Kairesalo and
Penttilΰ, 1990).
Although the general relationships between tem­
perature and egg and other developmental characteris­
tics of littoral and benthic cladocerans and copepods
are similar to those discussed earlier for planktonie
zooplankton (Chap. 16), several differences have been
found (e.g., Bottrell, 1975a,b; Sarvala, 1979). For ex­
ample, egg development time is increased markedly
with decreasing temperature, but among many species
of cladocerans and copepods, eggs of sessile species
take longer to develop than those of planktonie species,
regardless of temperature. Instar duration and fre­
quency of molting also tend to be greater among lit­
toral species than among planktonie species. Diurnal
migration has also been observed among zooplankton
living among macrophytes. During the day, many pop­
ulations, particularly copepods, aggregate among
macrophytes near the sediments (Szlauer, 1963; Kaire­
salo, 1980a). Portions of the populations may then mi­
grate to surface water strata during darkness.
Shallow lakes are often not sufficiently deep to
stratify thermally and are therefore unable to provide a
hypolimnetic refuge for zooplankton. In such waters,
distribution of zooplankton is highly variable between
littoral areas colonized by submersed aquatic plants
and the open pelagic region. As indicated earlier, in lit­
toral areas with well-developed aquatic macrophytes,
the cladocerans Alona, Chydorus, Diapbanosoma,
Bosmina, Ceriodaphnia and cyclopoid copepods are
usually more abundant per area of habitat, often by a
factor of 10, than in the pelagic areas (Vuille, 1991;
Paterson, 1993; Lauridsen and Buenk, 1996; Lauridsen
et al, 1996). Some cladocerans, such as Daphnia
magna, exhibited large diurnal changes, with highest
populations during the daytime among the submersed

macrophytes and movements into littoral boundary ar­
eas at night. Some species of cladocerans avoid sub­
mersed macrophytes, particularly during active photo­
synthesis periods, for unknown reasons (e.g., Dorgelo
and Heykoop, 1985).
Many of the observed differences among the abun­
dance of rotifers, cladocerans, and copepods within
plant beds and the open water likely reflect variations in
fish predation pressure (cf. further discussion in Chap.
20). The success of the habitat as a refuge for zooplank­
ton clearly is related to plant density. Additionally, the
size of zooplankton among submersed littoral vegeta­
tion tends to be larger than the size of zooplankton of
the pelagic zone, indicative of selective predation upon
larger forms. Daphnia species are commonly reduced to
very low population levels in open water but can persist
amongst extensive macrophyte stands after its elimina­
tion from open-water habitat. Daphnia is commonly
succeeded by other cladocerans, all of which maintain a
high grazing pressure on phytoplankton in the littoral
areas (e.g., Stansfield et al., 1997).
Although grazing pressures from small (0+-age
fry) zooplanktivorous fish are high, plant refuges are
significant. Based on correlational data from many
lakes, it is clear that predatory control of zooplankton
by planktivorous fish is reduced markedly in lakes rich
in submersed macrophytes, where at least ca. 1 5 - 2 0 %
of the water volume is occupied by submersed vegeta­
tion (Jeppesen et al., 1997; Persson and Crowder,
1998). Similar results can be demonstrated experimen­
tally in controlled enclosure experiments in shallow
lakes (e.g., Jeppesen et al., 1998). The large plants
serve as a refuge for pelagic cladocerans and encourage
predatory fish at the expense of prey fish that tend to
avoid dense littoral areas. Small planktivorous fish use
macrophytes as a defense mechanism against predators
and can compete effectively with predatory fish, partic­
ularly in the juvenile stages.
VI. SUMMARY
1. Benthic algae and cyanobacteria are generally
associated with or attached to substrata in land-
water interface habitats. These substrata are living
or dead, organic or inorganic, and in various com­
binations within the plants, detrital masses, and
sediments within emergent and submersed plant
zones and with sediments below macrophyte colo­
nization. Extremely diverse microhabitats occur in
littoral areas among substrates of sand, rock,
organic sediments, and macrophytes.
2. Limnological terminology applied to attached
microbiota refers to generic types of substrata to
VI. Summary 621
which groups of organisms are associated
(cf. Fig. 8-3, p. 131ff).
3. Attached algae of littoral communities often form
the dominant algal biomass in streams and shallow
lakes. Over 80% of all algal species likely grow
attached in submersed habitats.
a. Diatoms dominate on all substrata among
moderately productive aquatic ecosystems.
b. Sessile cyanobacteria and flagellates increase in
abundance in organically enriched lakes and
certain regions of streams.
4. Developing periphyton are three-dimensionally en­
meshed with hydrated mucopolysaccharide materi­
als, secreted by bacteria and algae, that both se­
quester ions and isolate the microorganisms from
the water column (Fig. 19-3). Accumulated detrital
particles and precipitated carbonates adsorb nutri­
ent ions and organic compounds. Some microbiota
are loosely attached and project within and above
the general community aggregations. The polysac-
charide matrix can contain microchannels that
likely function as conduits that allow accelerated
diffusion within the communities.
5. Resources regulating growth include both external
resources in the overlying medium, such as light
and nutrients in the surrounding water, and inter­
nal resources, such as nutrients that are obtained
from the substrata to which the periphyton com­
munities are attached.
a. Availability of habitat space markedly affects
the composite productivity of the periphytic
communities. Some habitats, such as many
sediments, are approximately two-dimensional
and provide much less surface area and have
much lower periphyton productivity than a
three-dimensional habitat, such as submersed
macrophytes. The epiphytic communities have
manifold greater productivity as the spatial
volume of the habitat projects upward into the
water column and enhanced light field (see
Fig. 19-8).
b. Enrichments of nutrients, particularly phospho­
rus and nitrogen, in the overlying water com­
monly result in shifts in species composition
and increases in growth and biomass of at­
tached algae on substrata. Within a specific
range of current velocities, the boundary layer
thickness between the periphyton and the over­
lying water is reduced with increasing current
velocities and results in enhanced nutrient ex­
change with the overlying water.
c. As communities develop and increase in thick­
ness, instability can occur and cells and
portions of the community may slough off.
622 19. Land- Water Interfaces: Attached Microorganisms, Littoral Algae, and Zooplankton
6. Many periphytic communities are dependent upon
the substrata for mineral and organic nutrients,
particularly from submersed macrophytes and in
oligotrophic and mesotrophic environments where
the greatest periphyton productivity occurs. As
macrophytes senesce and organic matter decom­
poses, a large portion of the nutrients and organic
substrates released are sequestered and intensively
recycled among the periphytic microbiota. This re­
tention is particularly effective in epiphytic and
epipelic periphyton.
7. A tight, mutualistic, metabolic coupling exists be­
tween attached algae and bacteria. For example,
bacterial production is increased by algal exudates
of organic substrates and oxygen. Enhanced algal
growth can occur from increased availability of
C 0 2 and growth factors such as vitamins and re­
duced oxygen tension. Nutrients are certainly recy­
cled and exchanged rapidly among the periphyton
microbiota.
8. Light availability influences periphyton production
both spatially along depth gradients and season­
ally. Even though benthic algae can adapt with in­
creased pigment concentrations to very low light
intensities, light is often restrictive not only with
increasing depth but seasonally, particularly
among low-order woodland streams that are heav­
ily canopied with terrestrial vegetation. Light is
attenuated selectively within periphyton as well,
and excessive developments of periphyton can
reduce light reaching sufficiently to kill the sup­
porting macrophytes and hence habitat space for
colonization.
9. Mortality losses among periphyton communities
are poorly known despite much study.
a. Heavy grazing of periphyton by animals (insect
larvae, crayfish, and certain fishes) can result in
reductions of periphytic biomass and productiv­
ity. Although most periphyton are not grazed by
animals, attached microbial-grazer interactions
and mortality vary with herbivore type, nutrient
and light availability for compensatory growth,
and disturbance frequency. There is some evi­
dence that grazing mortality of periphyton is
greater in stream ecosystems than in standing
waters.
b. Disturbance to the habitat of periphyton com­
munities can be severe from physical disrup­
tions of substrata, such as during river flooding,
and from shifts in water level, particularly
among shallow habitats. Algae living on loose
sediments that are subject to disturbance and
displacement by water movements and animals
often exhibit an ability to migrate vertically in
response to changes in light. This vertical mi­
gration is phased with diurnal rhythms in cell
division and photosynthetic capacity.
c. Losses of natural periphyton communities by
natural senescence and death, parasitism partic­
ularly by viruses, and disease are poorly known,
but it is apparent that most of the periphyton
production enters the pool of detrital organic
matter in both lake and river ecosystems.
10. In temperate regions, the seasonal community bio-
mass of attached algae commonly follows seasonal
changes in incident light and temperature.
a. Epipelic diatoms frequently exhibit population
maxima in the spring and in the autumn.
b. Seasonal population dynamics of epiphytic
algae are more variable and change as the
surface area available for colonization of the
supporting macrophytes changes seasonally.
11. Within the streams and rivers and the littoral zone
of standing waters, photosynthesis of attached al­
gae is influenced to a great extent by light avail­
ability, although compensatory mechanisms exist
that permit appreciable active growth at low levels
of irradiance.
a. The biomass of epipelic algae commonly in­
creases with increasing nutrient content of the
sediments.
b. Epipelic algae can utilize significant quantities
of phosphorus and combined nitrogen in the in­
terstitial water of sediments and alter, by photo-
synthetically changing sediment redox, the flux
of nutrients from the sediments to overlying
water in the littoral zone.
12. Where comparisons of growth among algal popu­
lations associated with different substrates are pos­
sible, they indicate that photosynthesis is com­
monly higher for algae attached to sand grains
than it is for those associated with organic sedi­
ments. Algae epiphytic on macrophytes are often
much more productive than algae associated with
sediments.
13. Productivity of littoral algae is not much greater
on a cellular basis than that of phytoplankton, and
turnover rates tend to be somewhat slower.
a. The large surface area available for coloniza­
tion, however, particularly on submersed
macrophytes, can result in very high contribu­
tions by attached littoral algae to the total pri­
mary productivity of many freshwater ecosys­
tems.
b. Spatial heterogeneity in rates of production by
attached algae is usually very large because of
the great variability in littoral habitats within
freshwater ecosystems.

e. Community rates of primary production of
attached algae commonly follow the annual in­
solation and temperature curves, with maxima
occurring in midsummer.
d. Most lakes of the world are shallow and pos­
sess large littoral zones. The productivity of the
littoral algae and macrophytes tends to increase
in relation to that of the phytoplankton as lakes
become enriched. In lakes with a modest devel­
opment of submersed macrophytes, epiphytic
productivity can be very high and dominate to­
tal in-lake photosynthetic productivity. Under
eutrophic conditions, excessive growth of phy­
toplankton and epiphytic algae can reduce light
sufficiently to cause the decline of submersed
macrophytes and attached algae; a consequent
overall reduction in total productivity within
the lake will then result.
14. Many of the protozoan, other protistan, rotifer,
and microcrustacean zooplankton of the littoral
zone are sessile on the sediments or macrophytes
and are not truly (or are only intermittently)
planktonie.
a. Plant-associated zooplankton are commonly
sessile on specific macrophyte types. Population
VI. Summary 623
densities of animals feeding on epiphytic mi­
croflora and detritus are positively correlated
with epiphytic algal density.
b. Many of the life history, reproductive, and
population characteristics of littoral-inhabiting
zooplankton are similar to those of their pelagic
counterparts.
15. In shallow lakes with a well-developed submersed
aquatic plant littoral area, the littoral habitat can
function as a refuge for zooplankton from fish and
invertebrate predation that prevails in the open
water.
a. Population numbers of common littoral micro-
crustaceans increase during spring and summer
and decrease during summer. Midsummer pop­
ulation minima often result from intense preda­
tion by insect larvae and small fishes.
b. Predatory control of zooplankton by planktivo-
rous fish is reduced markedly where minimally
1 5 - 2 0 % of the water volume is occupied by
submersed vegetation.
e. Zooplankton grazing can impact phytoplank­
ton within the littoral and contribute to reduced
phytoplankton and improved water trans­
parency.