Influence of the vertical structure of macrophytestands on epiphyte community metabolism
Chantal Vis, Christiane Hudon, and Richard Carignan
Abstract: The physical structure of submerged aquatic plant communities differentially influences the availability oflight and substratum in the water column and, thus, the functional role of epiphytes growing on macrophytes. We ex-amined the depth distribution of photosynthesis and respiration of epiphyte communities within macrophyte stands ofcontrasting growth forms over a 2-year period in Lake Saint-Pierre (St. Lawrence River). To do so, we used a model-ling approach, combining laboratory measurements of photosynthesis and respiration with field data of macrophyte andepiphyte biomass and vertical light attenuation. In stands dominated by canopy-forming macrophytes, shading resultedin strong vertical gradients in epiphyte metabolism, with a positive net oxygen balance in the canopy and a negativenet oxygen balance in the bottom portion of the stand. In low-growing macrophyte stands, the net oxygen balance ofepiphytes was either positive or negative, depending on water transparency and depth. Epiphyte communities had adaily negative net oxygen balance under light conditions below ~10% of surface light intensity. Areal production simu-lations demonstrated that neglecting variations in the vertical distribution of epiphytes, macrophytes, and light withinmacrophyte stands can result in errors in areal production estimates of >100%.
Résumé : La structure physique des communautés de plantes aquatiques submergées affecte de façon différentielle ladisponibilité de la lumière et des substrats dans la colonne d’eau et ainsi le rôle fonctionnel des épiphytes qui croissentsur les macrophytes. Nous avons mesuré la répartition de la photosynthèse et de la respiration des communautésd’épiphytes en fonction de la profondeur dans des peuplements de macrophytes présentant des formes de croissancedifférentes sur une période de deux ans au lac Saint-Pierre (fleuve Saint-Laurent). Pour ce faire, nous avons une ap-proche de modélisation qui combine des mesures de photosynthèse et de respiration en laboratoire à des données deterrain sur la biomasse des macrophytes et des épiphytes et sur l’atténuation verticale de la lumière. Dans les peuple-ments dominés par des macrophytes qui forment une canopée, l’ombrage cause de forts gradients verticaux de métabo-lisme des macrophytes, avec un bilan net d’oxygène positif dans la canopée et un bilan net d’oxygène négatif dans lapartie inférieure du peuplement. Dans les peuplements de macrophytes à formes de croissance basses, le bilan netd’oxygène est positif ou négatif selon la transparence et la profondeur de l’eau. Les communautés d’épiphytes ont unbilan journalier net d’oxygène négatif lorsque les conditions lumineuses sont grosso modo inférieures à 10 % del’intensité de la lumière en surface. Des simulations de production en fonction des sites montrent que d’ignorer lesvariations de répartition verticale des épiphytes, des macrophytes et de la lumière au sein des peuplements de plantesaquatiques peut causer des erreurs d’estimation de la production de plus de 100 % dans les différents sites.
[Traduit par la Rédaction] Vis et al. 1026
Introduction
The epiphyte community is a mixture of microalgae, bac-teria, fungi, inorganic particles, and detritus on the surfaceof submerged aquatic vegetation. Epiphytes can be importantcontributors to the primary production of wetlands, lakes,and rivers, thereby influencing ecosystem metabolism andtrophic dynamics (Wetzel 2001). Compared with the studyof phytoplankton, the study of metabolic rates by these at-tached communities presents additional difficulties linked tothe vertical and horizontal heterogeneity in biomass, substra-
tum availability, light levels, and turbulence across spatialscales ranging from micrometres to kilometres. Within macro-phyte stands, the physical vertical structure created by theplants influences light and substratum availability and thusthe biomass and productivity of epiphyte communities at-tached to macrophyte leaves and stems. Realistic estimatesof areal epiphyte community metabolism, which integratethe vertical irregularities in plant stands, are essential to deter-mining the importance of epiphytes at the whole-system level.
Depth variations in epiphyte biomass are interrelated withlight and wave action in macrophyte stands. Surface wave
Received 27 June 2005. Accepted 29 November 2005. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on12 April 2006.J18760
C. Vis1,2 and R. Carignan. Département de sciences biologiques, Université de Montréal, C.P. 6128, succ. Centre-Ville, Montréal,QC H3C 3J7, Canada.C. Hudon. St. Lawrence Centre, Environment Canada, 105 McGill Street, 7th Floor, Montreal, QC H2Y 2E7, Canada.
1Corresponding author (e-mail: [email protected]).2Present address: National Water Research Institute, Environment Canada, 867 Lakeshore Road, P.O. Box 5050, Burlington,ON L7R 4A6, Canada.
action can result in an increase in epiphyte biomass withdepth, whereas light attenuation leads to decreases inepiphyte biomass with depth (e.g., Kairesalo 1983; Lalondeand Downing 1991; Müller 1995). Photosynthetic rates ofattached algae vary as a function of the thickness of theepiphytic layer and light availability (e.g., Boston and Hill1991; Enriquez et al. 1996; Dodds et al. 1999). The depthdistribution of epiphyte biomass therefore directly influencesphotosynthesis and respiration rates and consequently totalproduction. Hart and Lovvorn (2000) found that assuming aconstant vertical distribution of epiphyte biomass could the-oretically over- or under-estimate epiphyte community pri-mary production (per m2 of bottom area) by up to 53%.Depth variations in photosynthetic response could furtherskew estimates of areal primary production as photosyn-thetic rates of the epiphyte layer vary with depth (Cattaneoand Kalff 1980; Kairesalo 1983; Müller 1995).
Distinct types of macrophytes support variable amounts ofepiphytes because of differences in plant density, architec-ture, leaf age, and leaf morphology (Burkholder and Wetzel1989; Lalonde and Downing 1991; Cattaneo et al. 1998).The biomass of macrophytes and its vertical distribution inthe water column influence the amount and location ofcolonizable surface area for epiphytes. Differing architectureamong types of macrophytes results in depth variations ofepiphyte biomass on emergent (e.g., Kairesalo 1983;Burkholder and Wetzel 1989; Müller 1995), floating-leaved(e.g., Romo and Galanti 1998), and submerged macrophytes(e.g., O’Neill Morin and Kimball 1983). Among submergedmacrophytes, the bulk of biomass is found near the surfacefor canopy-forming species, whereas basal rosette formswith linear leaves (such as Vallisneria americana) tend toconcentrate biomass near the bottom (Westlake 1964; Titusand Adams 1979), particularly in flowing waters. The un-even distribution of macrophyte biomass in the water col-umn also affects light intensity and quality and watermovements within the stand (e.g., Westlake 1964; Van derBijl et al. 1989; Vermaat et al. 2000), further impacting themetabolic rates of epiphyte communities.
The interaction between depth and macrophyte growthform varies over time with seasonal plant growth and speciessuccession, changing the vertical structure of macrophytebiomass distribution (Burkholder and Wetzel 1989). In earlysummer, macrophyte biomass is low and concentrated nearthe sediments. When macrophyte biomass reaches its sum-mer peak, the plant canopy is fully developed and may oc-cupy the entire water column. These vertical shifts in thelocation of the macrophyte biomass result in elevated dis-solved oxygen (DO) concentrations within the canopy andreduced [DO] in the subcanopy layer in summer comparedwith a vertically homogeneous distribution of DO in earlysummer (Frodge et al. 1990). In rivers, fluctuating water lev-els can also result in such covariation of depth andmacrophyte growth form through the concentration and ex-pansion of macrophyte biomass in a water column of vari-able depth. The effects of shifts in the vertical location ofmacrophyte biomass on epiphyte community metabolismhave received limited attention.
In this study, we investigate the effects of depth andmacrophyte growth form on the metabolism and areal pro-duction of epiphyte communities. Photosynthesis vs.
irradiance relationships and respiration rates derived fromlaboratory incubations were used to calculate field rates ofepiphyte primary production and respiration at various sites.Sites colonized by macrophytes with contrasting growthforms were studied over a 2-year period in Lake Saint-Pierre,a large fluvial lake of the St. Lawrence River. We first ex-amine how epiphyte community photosynthesis and respira-tion vary with depth and macrophyte growth form.Secondly, we determine the influence of depth and macro-phyte growth form on estimates of areal epiphyte primaryproduction and on daily net oxygen balance (per m2 of bot-tom area). A 1 m drop in water levels among years providedus with the opportunity to assess the effect of the interactionbetween water depth and macrophyte growth form on epi-phyte communities.
Materials and methods
Study siteLake Saint-Pierre is a large (~300 km2) broadening of the
St. Lawrence River (mean annual discharge of 11 500 m3·s–1)located 100 km downstream of Montréal, Canada (46°12′N,72°49′W). This portion of the river is shallow (mean depth <4 m) and exhibits a large degree of spatial heterogeneity inits water quality characteristics because of the presence ofdistinct water masses. Its gently sloping shores and nutrient-rich waters have favoured the development of large expansesof emergent and submerged rooted aquatic vegetation(macrophytes) covering approximately 80% of the lake’ssurface area (Vis et al. 2003).
We sampled three sites, one within each of the major wa-ter masses, between June and October of 2000 and 2001(Fig. 1; Table 1). Site 1, located in brown waters, rich in dis-solved organic carbon (DOC) and originating principally fromthe Ottawa River, supported a moderate biomass of low-growing Vallisneria americana with a sparse canopy ofPotamogeton richardsonii. Site 2, situated in relatively clearwaters flowing from Lake Ontario, was colonized byStuckenia pectinata (formerly Potamogeton pectinatus),forming a dense canopy in July, which was later succeededby Vallisneria americana (August). Site 3 (2001 only) wasunder the influence of brown and heavily enriched waters ofthe Yamaska River. This site, located in relatively shallowwater (<0.6 m), had a dense cover of Vallisneria americanaand Potamogeton richardsonii, interspersed with emergentvegetation (e.g., Schoenoplectus lacustris, Typha angus-tifolia). At all sites, macrophytes appeared in June andreached their maximum biomass in mid-August, with the ex-ception of Stuckenia pectinata, which reached its maximumbiomass in July and completely senesced in August.
Artificial substrataAt each site, we installed artificial substrata haphazardly
among natural plants (within a radius of 5 m) in early Juneof each year, coinciding with the spring emergence ofmacrophytes. Artificial substrata were made of ~3 cm ×10 cm (100 µm thick) clear polyethylene strips tied at 20 cmintervals to 1 to 3 m long strings of nylon monofilament.The strings were anchored to the bottom, and a cork tied tothe upper end maintained the artificial substrata vertical inthe water column. At site 3, plastic rods (diameter 0.85 cm)
Fig. 1. Map of study sites located in Lake Saint-Pierre (St. Lawrence River) overlying a black and white Landsat TM image (21 Septem-ber 1984), which shows the distribution of the major water masses. Site 1 (north water mass) and site 2 (central water mass) were sam-pled in 2000 and 2001, and site 3 (south water mass) was added in 2001.
VariableSite 1,north shore
Site 2,central
Site 3,south shore
Temperature (°C) 20.1 20.1 21.8(15.8–23.2) (14.7–23.8) (17.4–25.6)
Current velocity (m·s–1) 0.10 0.13 0.04(0–0.24) (0–0.40) (0–0.11)
Specific conductivity (µS·cm–1) 156 236 250(116–210) (138–289) (154–308)
(1.4–6.7) (0.8–5.7) (11.1–47.7)aMeasured only in 2000, C. Hudon, unpublished data.bMeasured only in 2001.
Table 1. Average characteristics of the study sites (range in parentheses) in Lake Saint-Pierre betweenJune and September of 2000 and 2001.
mimicking the stems of emergent vegetation were stuck intothe sediments. Artificial substrata permitted the use of theoxygen method to measure whole-assemblage gross produc-tion and dark respiration rates, without the interference ofthe host macrophyte.
Measurement of photosynthesis and respiration ratesPhotosynthesis (P) and respiration (R) were measured
monthly between June and September of each year. Sam-pling depth of artificial substrata was recorded by divers atthe time of collection (6 to 9 strings per site). Individualstrips used for P and R measurements were kept at in situtemperatures and processed within 6 h at a nearby field labo-ratory. The strips were incubated in 300 mL clear and darkPyrex bottles filled with filtered (Whatman GF/C) water col-lected on site. We ensured that all bottles used in a given ex-periment had identical (±0.01 mg·L–1) initial oxygenconcentrations by distributing the filtered water from a 20 Lpolyethylene tank in which a floating cover prevented gasexchange during the filling operation; water was delivered tothe bottom of each bottle, allowing for a two-volume over-flow. One plastic strip was inserted into each bottle (after re-moval of macroinvertebrates), and the bottles were placed ina temperature-regulated, rotating-wheel incubator (Shearer etal. 1985) equipped with a Philips MH1000 1000-watt metalhalide lamp. Duplicate or triplicate samples were incubatedat in situ temperatures (±1 °C) during 2–5 h under five lightintensities ranging from 20 to 1000 µmol·m–2·s–1. Commu-nity dark respiration (Rcom) was determined from the incuba-tion of artificial substrata in dark bottles. Photosyntheticallyactive radiation (PAR) was measured (Biospherical QSL-100quantum meter; Biospherical Instruments Inc., San Diego,California) at each level of light intensity (incubator wheel)during incubations. Initial DO concentration was determinedfrom triplicate clear bottles incubated without artificial sub-stratum. At the end of the incubation, DO concentration wasmeasured in each bottle using a YSI model 5905 self-stirringoxygen probe (YSI Incorporated, Yellow Springs, Ohio) cal-ibrated in water-saturated air at local barometric pressure.Plastic rods colonized within stands of emergent macrophyteswere cut into 5 cm segments and treated as above.
Net primary production (NPP) and Rcom were calculatedfrom the changes in oxygen concentration during incubation.Gross primary production (GPP) was calculated as NPP +Rcom. Epiphyte biomass on artificial substrata was deter-mined by extracting pigments directly from plastic strips orrods, frozen whole after incubation. Chlorophyll a (Chl a)was determined spectrophotometrically following 24 h ex-traction in 95% ethanol, using the equations of Nusch(1980), and was converted to mg Chl a·m–2 using the surfacearea of individual strips (length × width × 2) and rods (2πr ×height), assuming the entire surface of artificial substratawas available for colonization. Pmax, the maximum rate oflight-saturated gross photosynthesis, and α, the initial slope,were estimated from the fit of photosynthesis–irradiance(P–I) data to the hyperbolic function of Jassby and Platt(1976). Both photosynthetic parameters were expressed perunit biomass (P max
B , αB) and per unit area (P maxA , αA). The
light compensation point (Ic), or the irradiance at which pho-tosynthesis equals respiration, was calculated as Ic = Rα–1
(Enriquez et al. 1996).
Field measurementsEnvironmental conditions, stand characteristics, and
epiphyte biomass (on natural plants) were also measured ateach site, fortnightly between June and September of eachyear. Water temperature, conductivity, and pH (HydrolabMiniSonde 4a; Hydrolab, Austin, Texas) and current velocity(Marsh-McBirney FloMate model 2000; Marsh-McBirney,Frederick, Maryland) were measured 20 cm below the sur-face. Light (PAR) attenuation coefficients within macrophytestands were determined using a surface (LICOR LI-190SA;LICOR Corp., Lincoln, Nebraska) and submersible (LI-193SA) spherical sensor. Measurements were made withoutdisturbing the canopy by attaching the underwater light anda pressure sensor to the end of a pole that was loweredobliquely into the macrophyte stand. An average PAR atten-uation coefficient (Ktotal or Kt) for the water column, includ-ing the shading effect of dense macrophytes, was calculatedfrom three to six profiles at each site. Total water depth,macrophyte species composition, and average height andlength were also recorded on each sampling date.
To determine epiphyte biomass on natural plants (ex-pressed as µg Chl a·g–1 dry weight (DW) of plant), three tosix replicate samples (15 cm segment of macrophyte stemenclosed in a plexiglass cylinder (7.6 cm inside diameter))were collected fortnightly at each site at a single depth. Inthe laboratory, epiphytes were separated from the plant byvigorously shaking the plant fragment for 1 min in a 1 Lcontainer, and duplicate subsamples of the suspension werefiltered (Whatman GF/C) and frozen until extraction. Afterremoval of epiphytes, macrophytes were identified, dried toa constant mass (60 °C), and weighed.
The vertical distribution of epiphyte and macrophyte bio-mass was determined for individual plants. In July and Au-gust, entire plants were collected at sites 1 and 2 by a diver.Plants were divided into three segments of equal length (top,middle, bottom) and placed in a container. In the laboratory,epiphyte and macrophyte biomass of each segment was de-termined using the procedure outlined above.
We sampled macrophyte biomass between July and Au-gust (period of maximum biomass) of 2000 and 2001 alonga transect adjacent to our study sites. Plant biomass was as-sessed at fixed stations along the transect, with nine stationslocated near site 1 and 10 stations near site 2. At each sta-tion, replicate 25 cm × 25 cm quadrats (three to five) of allplant matter (above- and below-ground structures) were har-vested by divers. In the laboratory, macrophytes werecleaned to remove epiphytes and sediments, identified andseparated by species (aboveground only), dried to a constantmass (60 °C), and weighed. Average areal macrophyte bio-mass by site and by species was calculated. No measure-ments of macrophyte biomass were made at site 3, so weassumed that submerged macrophyte biomass was the sameas at site 1 and used the average value of emergent macro-phyte biomass for marsh habitats in Lake Saint-Pierre(C. Hudon, unpublished data).
Calculation of in situ photosynthesis and respirationTo examine the effects of variations in the depth distribu-
tion of epiphyte biomass and photosynthetic response on es-timates of epiphyte community production (per m2 ofbottom area), we modelled epiphyte primary production and
whole-community respiration. This was done at all sites forthe period of peak macrophyte biomass only (August), be-cause we did not measure seasonal changes in macrophytebiomass. At site 2, we also modelled areal epiphyte produc-tion in July, when Stuckenia pectinata dominated.
Time- and depth-integrated epiphyte photosynthesis(mg O2·m
–2·day–1) were calculated according to Jones (1984)or by using the numerical integration methods commonlyapplied to phytoplankton (Fee 1990). Daily photosynthesiswas modelled for an average square metre of macrophytehabitat by combining measures of (i) the depth distributionof epiphyton biomass B(z), (ii) the P–I curve (P max
B and αB),and (iii) irradiance at depth (Iz) based on light attenuationcoefficients and diurnal variations of surface irradiance. Spe-cifically, epiphytic primary production for an entire day (D,day length) over the entire water column to its maximumdepth (Zm) was calculated by numerical integration over depth(z by 0.1 m intervals) and time (t by 30 min intervals) as
(1) P ( )mg O m day2 ⋅ ⋅ =− −2 1
B z PI
Pz t
ZD z( ) tanh( )
maxmax
B0 B
md d∫∫
⎛
⎝⎜
⎞
⎠⎟
0
α
The depth distribution of epiphyte biomass (B(z), in mgChl a·m–2·(0.1 m depth stratum)–1) was modelled for eachsite by combining field data on mean macrophyte biomass(g DW·m–2), mean epiphyte biomass (µg Chl a·g–1 DW ofplant), the vertical distribution of each (as a percent of totalfor an individual plant), and observations of macrophytelength and height in the water column.
Hourly gross primary production within each 10 cm depthstratum was calculated as the product of epiphyte biomasswith the hourly photosynthetic rate at that depth (eq. 1).Photosynthetic parameters (P max
B and αB) were computed asa continuous function of epiphyte biomass (Chl a), based onthe linear regression relationships developed for Lake Saint-Pierre. Epiphyte biomass on natural macrophytes (per gramdry weight of plant) was converted to biomass per unit areaof substratum using the following surface area to biomassrelationships measured in Lake Saint-Pierre: 957 cm2·g–1 DWof Vallisneria americana, 1034 cm2·g–1 DW of Potamogetonrichardsonii, 993 cm2·g–1 DW of Stuckenia pectinata, and106 cm2·g–1 DW of emergent macrophytes.
Light intensity at depth (Iz) was modelled from time-dependent daily surface irradiance data (I0) and lightattenuation coefficients (Kt, including shading effects ofmacrophytes) as
(2) I IzK z= −
0 e t
We used average light attenuation coefficients measured inAugust (sites 1 and 3) or in July and August separately (site2) to account for the shift in dominance from Stuckeniapectinata to Vallisneria americana. Incident irradiance val-ues used in models were set at 60% of cloudless PAR for aday in July and August, which was calculated by 30 min in-tervals as a function of latitude and day of year (Fee 1990).We used an irradiance of 60% of cloudless PAR because thisvalue corresponded to the average daily PAR measured dur-ing 2000 and 2001. Surface irradiance at site 3 was esti-
mated as 20% of incident solar irradiance to account for theshading effects of the emergent canopy (Hudon 2004).
Epiphyte community respiration was assumed to occur ata constant rate throughout the day and over depth. Dailyrespiration was estimated as the product of mean hourlybiomass-specific respiration rates determined from incuba-tions (0.5 mg O2·(mg Chl a)–1·h–1) × 24 h × epiphyte bio-mass within each depth stratum. Areal (per m2 of bottom)primary production and respiration were determined by sum-ming over all depths for the entire day. Net oxygen balance(NET) was calculated as primary production minus respira-tion.
A sensitivity analysis was used to determine the responseof areal gross primary production, respiration, and net oxy-gen balance of epiphyte communities to changes inmacrophyte biomass, epiphyte biomass, and light attenuationcoefficients. In the analysis, each of the independent vari-ables was subjected to 0.5- and 2-fold variation. We alsocompared the estimates of areal primary production calcu-lated using numerical integration with estimates obtainedfrom a single surface sample. Productivity rates (mg O2·g
–1
DW·day–1) obtained within 10 cm of the surface (or in thefirst 10 cm from the top for Vallisneria) were multiplied bymean macrophyte biomass (g DW·m–2) to calculate arealdaily production.
Results
Photosynthetic parameters and dark respiration measure-ments from artificial substrata immersed at various waterdepths and light conditions reflect the broad range of sea-sonal and interannual fluctuations in physical conditions (Ta-ble 2). Epiphyte communities exhibited typical lightsaturation curves, without photoinhibition for irradiances upto 1000 µmol·m–2·s–1, and the hyperbolic tangent P–I func-tion fit the photosynthetic data well (goodness of fit r2 =0.78–1.00). Despite varying chemical and physical charac-teristics among sites (Table 1), photosynthetic parametersand dark respiration of epiphyte communities were moststrongly related to each other and to biomass. Pmax and αwere positively correlated with each other, whether ex-pressed per unit biomass (r = 0.55, p = 0.007, n = 23) or perunit surface area of substratum (r = 0.74, p < 0.0001, n =23). Photosynthetic parameters were also positively corre-lated with Rcom (r = 0.55–0.90, p < 0.008).
When expressed per unit biomass, Pmax and α were nega-tively related to epiphyte biomass (Fig. 2, left column),whereas areal rates of both photosynthesis and dark respira-tion were positively correlated to epiphyte biomass (Fig. 2,right column). Biomass-specific dark respiration rates wereindependent of epiphyte biomass on artificial substrata (r =–0.33, p = 0.12, n = 23) and not correlated with light ordepth. The slope of the P–I curve (α) was not correlatedwith depth but showed significant relationships with light;correlations were positive for biomass-specific rates (r =0.41, p = 0.05) and negative for areal rates (r = –0.39, p =0.06). Light compensation point (i.e., the intensity at whichP equals R) ranged from 10 to 308 µmol·m–2·s–1; it increasedwith sampling depth (r = 0.44, p = 0.04) and decreased withlight (r = –0.52, p = 0.01).
Depending on growth form, macrophyte biomass wasconcentrated near the bottom for basal rosette forms (i.e.,Vallisneria) or in the upper portion of canopy-forming spe-cies (Fig. 3), consistent with previous studies (Westlake1964; Titus and Adams 1979). The vertical distribution ofepiphyte biomass on macrophytes, as a percentage of totalbiomass, also differed between growth forms and positionin the water column (two-way analysis of variance,ANOVA, p = 0.0048), being highest in the upper portion ofVallisneria and in the middle part of canopy-forming spe-cies in summer (Fig. 3). The vertical distribution of totalepiphyte biomass was similar for both growth forms, dem-onstrating a decrease in Chl a with depth. Average epiphytebiomass on natural macrophytes (mean = 8 mg Chl a·m–2)was generally lower than on artificial substrata (mean =37 mg Chl a·m–2), although values covered the same range(0.5–158 mg Chl a·m–2).
Field measurements of macrophyte biomass, epiphyte bio-mass, and light attenuation were combined with laboratorydata of photosynthesis and respiration to model the depthdistribution of epiphyte gross primary production and whole-community respiration (Table 3; Fig. 4). Site-specific esti-mates were made for the period of peak biomass of Stuckeniapectinata (in July at site 2) and of other macrophyte species(in August at the three sites) in 2000 and 2001.
Epiphyte biomass on natural substrata differed significantlyamong sites (p = 0.0024), without significant differences be-tween macrophyte growth forms, years, and their interaction
terms. Gross primary production, respiration, and NET ofepiphytes were strongly related to macrophyte biomass,growth form, and light conditions, with marked differencesbetween sites and years (Fig. 4; Table 3). As expected, apattern of decreasing primary production with depth was ob-served. In canopy-forming stands, epiphyte assemblages inthe top half of the stand had a positive NET, which shiftedtowards negative values as one moved downwards within thestand. In stands dominated by basal rosette forms and linearleaves, NET of epiphyte communities depended primarily onlight conditions and could be either positive or negative. Atall sites, a daily negative NET of the epiphyte communitieswas found below roughly 10% of surface light intensity.
Epiphyton primary production was 1.5–5.5 times greaterunder low water levels (2001) than under the average levelconditions observed in 2000. The 1 m drop in water levelsand reduced water depth led to compression of the canopynear the surface in 2001, resulting in better overall light con-ditions and a positive NET for epiphytes. This increase be-tween years was due to the interactions between water depthand growth form, as light attenuation coefficients, arealmacrophyte, and epiphyte biomass did not vary significantlybetween 2000 and 2001 (Table 3).
A sensitivity analysis revealed that changes in the biomassof macrophytes (available surface area) would result in vari-ations in epiphyte biomass and areal primary production ofthe same order of magnitude (Table 4). Results are shownfor site 2 only, as similar trends were observed for the other
Note: Saturation photosynthetically active radiation (PAR; Ik) and the light compensation (Ic) are indicated for each series of measurements. Chl a, chlo-rophyll a; Pmax, the maximum rate of light-saturated gross photosynthesis; Rcom, community dark respiration. α is expressed in mg O2·mg Chl a–1·h–1·(µmol·m–2·s–1)–1. Both Pmax and Rcom are measured in mg O2·mg Chl a–1·h–1; both Ik and Ic are expressed in µmol·m–2·s–1.
aMeasurements made on plastic rods.
Table 2. Parameters of photosynthesis–irradiance (P–I) response curves for all incubations.
Fig. 2. Relationships between attached algal biomass and photosynthetic parameters (maximum rate of light-saturated gross photosyn-thesis (Pmax), initial slope (α), and community dark respiration (Rcom)), expressed either per unit of biomass (a, c, e) or per unit of sur-face area of substratum (b, d, f) for algal communities on artificial substrata. Data are coded by site. Linear relationships and equationsderived from least square regressions are indicated on each graph (n = 23). Chl a, chlorophyll a.
two sites (not shown). Despite similar impacts on areal epi-phyte biomass, altering epiphyte biomass (i.e., the thicknessof the community) had a differing effect on primary produc-
tion and NET compared with changing macrophyte biomass,because photosynthetic rates vary as a function of thickness.Changes in macrophyte biomass impacted the amount of
Fig. 3. Average vertical distribution of macrophyte and epiphyte biomass (expressed as a percentage of the total) between the top(TOP), middle (MID), and bottom (BOT) sections of basal rosette form Vallisneria americana (n = 7) and canopy-forming speciesPotamogeton richardsonii and Stuckenia pectinata (n = 2) collected in Lake Saint-Pierre. Significant differences between macrophytesections are indicated by different lowercase letters a and b above bars (Tukey–Kramer honestly significant difference test). Chl a,chlorophyll a; DW, dry weight.
Site 1 Site 2 Site 3
August July August August
Site characteristics 2000 2001 2000 2001 2000 2001 2001Depth (m) 1.7 0.7 3.0 1.3 2.0 1.1 0.5Light attenuation coefficient of water
and macrophytes (Kt, m–1)2.8 3.2 2.85 2.85 1.0 above V
4.5 within V
5.0
Light reaching the bottom (% of surfaceirradiance)
Table 3. Data used for field calculations of photosynthesis and respiration based on measured site characteristics (depth, light, andmacrophyte and epiphyte biomass) and model-derived estimates of epiphyte community gross daily production (GPP), dark respiration(Rcom), and net oxygen balance (NET).
surface available for epiphyte colonization without affectingphotosynthetic rates. Doubling epiphyte biomass per gramdry weight of plant decreased the photosynthetic efficiencyof the community (lower P max
B and αB), thus yielding amarkedly negative NET. In contrast, reduction of epiphytebiomass enhanced gross primary production because of in-creased photosynthetic rates with lower epiphyte loads.Variations in light conditions had the strongest influence onthe depth distribution of NET and on overall water-columntotal NET (Table 4). A single surface measurement of epi-phyte primary production (per m2 of substratum) extrapo-lated to an areal rate on the basis of average availability ofsubstratum per unit area of bottom overestimated epiphyteproduction in 9 out of 10 cases. The error factors induced byextrapolation ranged from 1.3 to 3, depending on macro-phyte species (growth form) and total depth (Table 5).
Discussion
Our results show how the depth distribution of epiphytebiomass, primary production, and community respirationand the resulting NET of the whole assemblage vary inmacrophyte stands of differing growth forms and under vari-able light conditions. Although photosynthetic parameterswere most strongly related to epiphyte biomass, the positionof the epiphyte layer within the macrophyte canopy and light
conditions had a major influence on depth-integrated dailyproduction by epiphytes. As such, a modelling approachconsidering the physical structure of macrophyte stands(growth form, distribution of biomass), light attenuation,vertical epiphyte biomass distribution, and P–I curve re-sponses of epiphytes is required to provide realistic estimateof epiphyte community metabolism in aquatic systems withmacrophytes (Jones 1984).
Metabolic rates of attached algaeWhole-assemblage photosynthetic and respiration rates
measured in this study using artificial substrata were consis-tent with previously reported values for attached communi-ties (e.g., Boston and Hill 1991; Goldsborough andRobinson 1996; Dodds et al. 1999), including studies usingepiphyte communities occurring on real macrophytes (Jonesand Adams 1982; Meulemans 1988). Average epiphyte bio-mass on artificial substrata was higher than on natural sub-strata; however, biomass was highly variable on both typesof substratum, showing an average coefficient of variationamong replicates of 45%. The relationships that we foundbetween photosynthetic rates, dark respiration, and biomassbased on measurements made on artificial substratum werealso in agreement with those of other studies (Boston andHill 1991; Enriquez et al. 1996; Dodds et al. 1999) and were
Fig. 4. Model-derived vertical distributions of net oxygen balance (NET) for epiphyte communities at three sites with different types ofmacrophyte stands in Lake Saint-Pierre: Vallisneria americana, V, black circles, solid lines; Potamogeton richardsonii, P, open circles,dotted lines; Stuckenia pectinata, S, open triangles, solid lines; and emergent vegetation, E, open squares, dotted line). Net primaryproduction integrated over the entire water column (Σ) is indicated on each panel by macrophyte species. Water levels in 2001 wereapproximately 1 m lower than in 2000; the bottom is represented by a hatched line in 2001.
useful for modelling the photosynthetic response of attachedalgae a function of biomass (Chl a). The P–I data providedin this study add to the relatively sparse literature on peri-phyton photosynthesis (Vadeboncoeur and Steinman 2002).
Laboratory-derived measurements of photosynthesis re-vealed changes in the photosynthetic response of attached al-gae with depth and light. Photosynthetic efficiency per unitarea decreased with light intensity (conversely, increasedwith depth). In contrast, photosynthetic efficiency per unitbiomass increased with light (decreased with depth). Theserelationships were more apparent with light conditions (lowsignificance) than with depth (not significant). Althoughlight and depth were negatively correlated (r = –0.47, p =0.02), the presence of plant canopies resulted in a widerange in light levels (10% and 60%) at a given depth, whichcould explain the lack of significant relationships with
depth. The poor correspondence between depth and lightintensity within dense macrophyte canopies was previouslyreported by Gosselain et al. (2005). Weak correlations be-tween photosynthetic efficiency and light (depth) could alsobe partly explained by the wide daily fluctuations in waterlevels (up to 37 cm) between consecutive days in this riversystem.
Studies on macrophytes have shown variable respirationrates with depth, with respiration rates being lowest in thebasal parts of Potamogeton (Van der Bijl et al. 1989). Bacte-rial production within attached microbial communities hasbeen found to be lower in the dark compared with in lightincubations (Espeland et al. 2001). In this study, no signifi-cant relationships could be discerned between Rcom rates andlight or depth. Respiration measurements on artificial sub-strata did demonstrate a positive relationship with Pmax and
Note: Chl a, chlorophyll a; DW, dry weight. ΣGPP, ΣRcom, and ΣNET are all expressed in mg O2·m–2·day–1.
aPhotosynthetic rates of epiphytes same as in original data.bPhotosynthetic parameters of epiphytes recalculated as thickness of community changed.
Table 4. Sensitivity of model-derived areal rates of epiphyte community gross daily primary production (GPP), dark community respi-ration (Rcom), and NET oxygen balance to variations in macrophyte and epiphyton biomass and light conditions at site 2 in July andAugust of 2000.
GPP (mg O2·m–2·day–1)
Year Site Month Macrophyte speciesDepthintegrated
Surfacesample
Errorfactor
2000 1 August Vallisneria americana 395 1175 3.0Potamogeton richardsonii 452 722 1.6
2 July Stuckenia pectinata 1106 3155 2.8August Vallisneria americana 532 1476 2.8
2001 1 August Vallisneria americana 2166 3495 1.6Potamogeton richardsonii 710 719 1.0
2 July Stuckenia pectinata 2484 3155 1.3August Vallisneria americana 868 1639 1.9
3 August Vallisneria americana 374 826 2.2Emergent species 105 210 2.0
Table 5. Comparison of estimates of areal epiphyte community gross primary production (GPP per m2 of bot-tom area) calculated from numerical integration over depth and time, taking into consideration vertical irregu-larities in the depth distribution of light and epiphyte and macrophyte biomass, and from a single surfacemeasurement of production extrapolated to m2 of bottom area (see text for details).
α, and decreased photosynthetic activity in the deeper part ofstands may be linked with decreased respiration. Futurestudies should examine the vertical distribution of heterotro-phic activities and assess DOC processing within macro-phyte stands.
Oxygen balance of epiphyte assemblagesOur study showed that light conditions, resulting from the
combination of macrophyte biomass and canopy structure,depth, and water transparency, exert a predominant influenceon the NET of epiphyte communities. Results further indi-cated a negative NET in epiphyte layers exposed to low orpoor light intensity, which are typical of the deeper portionof macrophyte stands in the St. Lawrence River. The averagelight compensation point (i.e., the irradiance at which photo-synthesis equalled respiration, 67 µmol·m–2·s–1) observed inour study was well within the previously reported range of7–80 µmol·m–2·s–1 (Hill 1996), but in the low part of therange (51–620 µmol·m–2·s–1) reported by Dodds et al.(1999). High values of light compensation points reflect theabundance of heterotrophs within the epiphyte layer(McIntire and Phinney 1965).
On a typical summer day with incident irradiation equal to1200 µmol·m–2·s–1, a positive NET could only be maintainedabove 6% of the surface light intensity; however, this calcu-lation is based on light compensation points for the photo-synthetically active period alone. Model-derived resultsshowed that epiphyte communities in this system could onlymaintain a daily (or 24 h day) positive NET above roughly10% of the average surface irradiance. In Lake Saint-Pierre,large portions of the water column receive less than 10% ofsurface irradiance because of turbidity and shading by plants.
The common occurrence of significant epiphyte biomassunder light conditions insufficient to maintain a positive ox-ygen balance thus seems paradoxical. Sand-Jensen et al.(1985) reported that natural epiphyte communities wouldlikely rarely have a negative NET and only under conditionsof extreme shading. One possible explanation for the nega-tive oxygen balance may be that DOC subsidies fromupstream or within the sediments maintained the net hetero-trophy of epiphytes, but this is unlikely the case in LakeSaint-Pierre. In this system, the organic content of sedimentsis <2% on average, and DOC concentrations do not varywithin a given water mass (i.e., along conductivity isolines)(C. Hudon, unpublished data). We suggest two other hypoth-eses to explain the negative NET of epiphyte communities:(i) seasonal changes in canopy density and shading condi-tions, and (ii) short-term variations in light conditions.
First, light conditions to which epiphyte communitieswere exposed could have progressively deteriorated over thesummer because of seasonal macrophyte growth. We calcu-lated that in early June, when macrophytes begin to grow,light conditions were favourable at all sites as >12% of sur-face irradiance reached the bottom. This would result in apositive NET of epiphyte communities in the early part ofthe growing season. Sand-Jensen et al. (1985) observed suchchanges in epiphytic communities in a Danish river, whichshifted from algal-dominated in spring to bacteria-dominatedassemblages in the summer when self-shading was highwithin dense macrophyte stands. The growth form of the
macrophytes influences epiphyte biomass accumulation(Burkholder and Wetzel 1989), and as such, apical growth inPotamogeton species could also account for the negativeNET of the epiphyte communities in the older, deeper partof the stem of these macrophytes.
Second, average light conditions used in our models maynot have been representative of the short-term variations inlight intensity, resulting in an underestimation of gross pri-mary production. Epiphyte communities maintain a high sat-uration PAR (Ik) despite being predominantly exposed to lowlight conditions, which may indicate that they are able toharness rare (i.e., sunflecks) or seasonal episodes of highirradiances (Hill 1996). Riverine habitats experiencing fluc-tuating water levels and discharge also induce variations inlight penetration within macrophyte stands moving with thecurrent. A dynamic light model may have better captured netoxygen dynamics of epiphyte communities exposed to inter-mittent flashes of higher light intensities.
Environmental effects between sites and years onepiphyte production
Differences in the environmental variables between sitesand years had little direct influence on epiphyte photo-synthetic parameters; however, habitat characteristics didimpact areal epiphyte production, respiration, and NET.Contrary to expectations, the shallowest sites (sites 1 and 3)were not the sites with the highest epiphyte production inthis system; these sites were found in coloured and turbidwaters with reduced light transparency. So despite being thearea with the highest availability of substratum per m2 ofbottom, areal epiphyte production was lower at sites 1 and 3compared with site 2, an area influenced by relatively clearwaters originating in the Great Lakes. Both availability ofsubstratum and light conditions are important factors to con-sider in large fluvial systems when estimating contributionsof epiphyte communities to whole-system production.
Low water levels in 2001 led to increases in oxygen pro-duction by epiphyte communities through the interactionsbetween depth, macrophyte growth form, and light condi-tions. Water depth and light intensity in the water column ofrivers are directly linked, and a 1 m drop in water levels re-sulted in more light reaching the bottom and a positive NETof epiphyte communities. Reduced water depths and theconcentration of the macrophyte biomass near the surfaceunder higher light intensity also caused an increase in oxy-gen production by epiphytes. Greater amounts of macro-phyte biomass located within the upper stratum of the watercolumn may lead to marked oxygen gradients between theupper and lower parts of the water column and can inducelow oxygen concentrations in bottom waters during the night(Frodge et al. 1990; Caraco and Cole 2002). Epiphyte com-munity metabolism contributes to these DO gradients in thewater column, as communities located at low light levelsdeep in the water column had a negative NET.
Implications on estimates of areal epiphyton productionWe found depth-related variations in areal epiphyte pri-
mary production resulting from the stratified distribution ofthe macrophyte and epiphyte biomasses and from unevenlight levels. Because areal rates (per m2 of substratum) are
extrapolated upwards to total macrophyte surface area avail-able (m2 of substratum per m2 of bottom area), the calcula-tion of total daily areal production (per m2 of littoral zone)from single-depth measurements can lead to over- or under-estimation of production rates, depending on samplingdepth. For example, simulations in this study show that sin-gle surface samples would lead to an overestimated arealproduction in 9 out of 10 cases, by factors ranging from 1.3to 3, depending on macrophyte growth form and waterdepth. The effects of vertical variations in epiphyte biomasson the calculation of areal production are dependent on lightlevels (Hart and Lovvorn 2000), and this study showed thatdepth variations in the photosynthetic response of epiphytescan also influence areal production. Because light conditionsvary daily and with depth, the extrapolation of in situ mea-surements of epiphyte production may be further subject toerror simply because of weather conditions on the day ofsampling. Temporal changes in depth distribution ofmacrophyte biomass and light must also be taken into ac-count when scaling-up measures of productivity to estimateannual epiphyte community production (Burkholder andWetzel 1989). This study demonstrates the importance of thevertical structure of macrophyte stands on the metabolism ofepiphyte communities, which must be considered to ade-quately assess whole-system production.
Acknowledgments
We thank A-M. Blais, M. Hugues, D. Poulin, and L.Robichaud and the Pourvoirie Gladu for help in the field andlab. We also thank V. Gosselain for the surface to biomassmacrophyte conversion data. A. Cattaneo, R. Maranger, andtwo anonymous reviewers provided valuable comments onthe manuscript. This study was supported by EnvironmentCanada (Centre Saint-Laurent), a Natural Sciences and Engi-neering Research Council of Canada (NSERC) researchgrant to R.C., and a Fonds pour la Formation de Chercheurset l’Aide à la Recherche (FCAR) scholarship to C.V.
References
Boston, H.L., and Hill, W.R. 1991. Photosynthesis–light relationsof stream periphyton communities. Limnol. Oceanogr. 36: 644–656.
Burkholder, J.M., and Wetzel, R.G. 1989. Epiphytic microalgae onnatural substrata in a hardwater lake: seasonal dynamics of com-munity structure, biomass and ATP content. Arch. Hydrobiol.83(Suppl.): 1–56.
Caraco, N.F., and Cole, J.J. 2002. Contrasting impacts of a nativeand alien macrophyte on dissolved oxygen in a large river. Ecol.Appl. 12: 1496–1509.
Cattaneo, A., and Kalff, J. 1980. The relative contribution ofaquatic macrophytes and their epiphytes to the production ofmacrophyte beds. Limnol. Oceanogr. 25: 280–289.
Cattaneo, A., Galanti, G., Gentinetta, S., and Romo, S. 1998. Epi-phytic algae and macroinvertebrates on submerged and floating-leaved macrophytes in an Italian lake. Freshw. Biol. 39: 725–740.
Dodds, W.K., Biggs, B.J.F., and Lowe, R.L. 1999. Photosynthesis–irradiance patterns in benthic microalgae: variations as a func-tion of assemblage thickness and community structure. J.Phycol. 35: 42–53.
Enriquez, S., Duarte, C.M., Sand-Jensen, K., and Nielsen, S.L.1996. Broad-scale comparison of photosynthetic rates acrossphototrophic organisms. Oecologia, 108: 197–206.
Espeland, E.M., Francoeur, S.N., and Wetzel, R.G. 2001. Influenceof algal photosynthesis on biofilm bacterial production and asso-ciated glucosidase and xylosidase activities. Microb. Ecol. 42:524–530.
Fee, E.J. 1990. Computer programs for calculating in situ phyto-plankton photosynthesis. Can. Tech. Rep. Fish. Aquat. Sci.No. 1740.
Frodge, J.D., Thomas, G.L., and Pauley, G.B. 1990. Effects of can-opy formation by floating and submergent aquatic macrophyteson the water quality of two shallow Pacific Northwest lakes.Aquat. Bot. 38: 231–248.
Goldsborough, L.G., and Robinson, G.G.C. 1996. Patterns inwetlands. In Algal ecology: freshwater benthic ecosystems.Edited by R.J. Stevenson, M.L. Bothwell, and R.L. Lowe. Aca-demic Press, San Diego, Calif. pp. 77–117.
Gosselain, V., Hudon, C., Cattaneo, A., Gagnon, P., Planas, D., andRochefort, D. 2005. Physical variables driving epiphytic algalbiomass in a dense macrophyte bed of the St. Lawrence River(Quebec, Canada). Hydrobiologia, 534: 11–22.
Hart, E.A., and Lovvorn, J.R. 2000. Vegetation dynamics and pri-mary production in saline, lacustrine wetlands of a RockyMountain basin. Aquat. Bot. 66: 21–39.
Hill, W. 1996. Effects of light. In Algal ecology. Edited by R.J.Stevenson, M.L. Bothwell, and R.L. Lowe. Academic Press, SanDiego, Calif. pp. 121–148.
Hudon, C. 2004. Shift in wetland plant composition and biomassfollowing low-level episodes in the St. Lawrence River: lookinginto the future. Can. J. Fish. Aquat. Sci. 61: 603–617.
Jassby, A.D., and Platt, T. 1976. Mathematical formulation of therelationship between photosynthesis and light for phytoplankton.Limnol. Oceanogr. 21: 540–547.
Jones, R.C. 1984. Application of primary production model toepiphytic algae in a shallow, eutrophic lake. Ecology, 65: 1895–1903.
Jones, R.C., and Adams, M.S. 1982. Seasonal variations inphotosynthetic response of algae epiphytic on Myriophyllumspicatum L. Aquat. Bot. 13: 317–330.
Kairesalo, T. 1983. Dynamics of epiphytic communities onEquisetum fluviatile L. In Periphyton of freshwater ecosystems.Edited by R.G. Wetzel. Dr. W. Junk Publishers, The Hague,Netherlands. pp. 153–160.
Lalonde, S., and Downing, J.A. 1991. Epiphyton biomass is relatedto lake trophic status, depth and macrophyte architecture. Can. J.Fish. Aquat. Sci. 48: 2285–2291.
McIntire, C.D., and Phinney, H.K. 1965. Laboratory studies ofperiphyton production and community metabolism in lotic envi-ronments. Ecol. Monogr. 35: 237–258.
Meulemans, J.T. 1988. Seasonal changes in biomass and produc-tion of periphyton growing upon reed in Lake Maarsseveen I.Arch. Hydrobiol. 112: 21–42.
Müller, U. 1995. Vertical zonation and production rates of epi-phytic algae on Phragmites australis. Freshw. Biol. 34: 69–80.
Nusch, E.A. 1980. Comparison of different methods for chloro-phyll and phaeopigment determination. Archiv Hydrobiol. Beih.Ergebn. Limnol. 14: 14–36.
O’Neill Morin, J., and Kimball, K.D. 1983. Relationships ofmacrophyte-mediated changes in the water column toperiphyton composition and abundance. Freshw. Biol. 13: 403–414.
Romo, S., and Galanti, G. 1998. Vertical and seasonal distributionof epiphytic algae on water chestnut (Trapa natans). Arch.Hydrobiol. 141: 483–504.
Sand-Jensen, K., Revsbech, N.P., and Barker Jorgensen, B. 1985.Microprofiles of oxygen in epiphyte communities on submergedmacrophytes. Mar. Biol. 89: 55–62.
Titus, J.E., and Adams, M.S. 1979. Coexistence and the compara-tive light relations of the submersed macrophytes Myriophyllumspicatum L., and Vallisneria americana Michx. Oecologia, 40:273–286.
Vadeboncoeur, Y., and Steiman, A.D. 2002. Periphyton function inlake ecosystems. Sci. World J. 2: 1449–1468.
Van der Bijl, L., Sand-Jensen, K., and Hjermind, A.L. 1989. Photo-synthesis and canopy structure of a submerged plant,Potamogeton pectinatus, in a Danish lowland stream. J. Ecol.77: 947–962.
Vermaat, J.E., Santamaria, L., and Roos, P.J. 2000. Water flowacross and sediment trapping in submerged macrophyte beds ofcontrasting growth form. Arch. Hydrobiol. 148: 549–562.
Vis, C., Hudon, C., and Carignan, R. 2003. An evaluation of ap-proaches used to determine the distribution and biomass ofemergent and submerged aquatic macrophytes over large spatialscales. Aquat. Bot. 77: 187–201.
Westlake, D.F. 1964. Light extinction, standing crop and photosyn-thesis within weed beds. Verh. Int. Verein. Limnol. 15: 415–425.
