1014
Influence of the vertical structure of macrophyte stands on epiphyte community metabolism Chantal Vis, Christiane Hudon, and Richard Carignan
Abstract: The physical structure of submerged aquatic plant communities differentially influences the availability of light and substratum in the water column and, thus, the functional role of epiphytes growing on macrophytes. We examined the depth distribution of photosynthesis and respiration of epiphyte communities within macrophyte stands of contrasting growth forms over a 2-year period in Lake Saint-Pierre (St. Lawrence River). To do so, we used a modelling approach, combining laboratory measurements of photosynthesis and respiration with field data of macrophyte and epiphyte biomass and vertical light attenuation. In stands dominated by canopy-forming macrophytes, shading resulted in strong vertical gradients in epiphyte metabolism, with a positive net oxygen balance in the canopy and a negative net oxygen balance in the bottom portion of the stand. In low-growing macrophyte stands, the net oxygen balance of epiphytes was either positive or negative, depending on water transparency and depth. Epiphyte communities had a daily negative net oxygen balance under light conditions below ~10% of surface light intensity. Areal production simulations demonstrated that neglecting variations in the vertical distribution of epiphytes, macrophytes, and light within macrophyte 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 la disponibilité de la lumière et des substrats dans la colonne d’eau et ainsi le rôle fonctionnel des épiphytes qui croissent sur les macrophytes. Nous avons mesuré la répartition de la photosynthèse et de la respiration des communautés d’épiphytes en fonction de la profondeur dans des peuplements de macrophytes présentant des formes de croissance différentes sur une période de deux ans au lac Saint-Pierre (fleuve Saint-Laurent). Pour ce faire, nous avons une approche de modélisation qui combine des mesures de photosynthèse et de respiration en laboratoire à des données de terrain sur la biomasse des macrophytes et des épiphytes et sur l’atténuation verticale de la lumière. Dans les peuplements dominés par des macrophytes qui forment une canopée, l’ombrage cause de forts gradients verticaux de métabolisme des macrophytes, avec un bilan net d’oxygène positif dans la canopée et un bilan net d’oxygène négatif dans la partie inférieure du peuplement. Dans les peuplements de macrophytes à formes de croissance basses, le bilan net d’oxygène est positif ou négatif selon la transparence et la profondeur de l’eau. Les communautés d’épiphytes ont un bilan journalier net d’oxygène négatif lorsque les conditions lumineuses sont grosso modo inférieures à 10 % de l’intensité de la lumière en surface. Des simulations de production en fonction des sites montrent que d’ignorer les variations de répartition verticale des épiphytes, des macrophytes et de la lumière au sein des peuplements de plantes aquatiques 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, bacteria, fungi, inorganic particles, and detritus on the surface of submerged aquatic vegetation. Epiphytes can be important contributors to the primary production of wetlands, lakes, and rivers, thereby influencing ecosystem metabolism and trophic dynamics (Wetzel 2001). Compared with the study of phytoplankton, the study of metabolic rates by these attached communities presents additional difficulties linked to the vertical and horizontal heterogeneity in biomass, substra-
tum availability, light levels, and turbulence across spatial scales ranging from micrometres to kilometres. Within macrophyte stands, the physical vertical structure created by the plants influences light and substratum availability and thus the biomass and productivity of epiphyte communities attached to macrophyte leaves and stems. Realistic estimates of areal epiphyte community metabolism, which integrate the vertical irregularities in plant stands, are essential to determining the importance of epiphytes at the whole-system level. Depth variations in epiphyte biomass are interrelated with light 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 on 12 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. 1 2
Corresponding author (e-mail:
[email protected]). Present address: National Water Research Institute, Environment Canada, 867 Lakeshore Road, P.O. Box 5050, Burlington, ON L7R 4A6, Canada.
Can. J. Fish. Aquat. Sci. 63: 1014–1026 (2006)
doi:10.1139/F06-021
© 2006 NRC Canada
Vis et al.
action can result in an increase in epiphyte biomass with depth, whereas light attenuation leads to decreases in epiphyte biomass with depth (e.g., Kairesalo 1983; Lalonde and Downing 1991; Müller 1995). Photosynthetic rates of attached algae vary as a function of the thickness of the epiphytic layer and light availability (e.g., Boston and Hill 1991; Enriquez et al. 1996; Dodds et al. 1999). The depth distribution of epiphyte biomass therefore directly influences photosynthesis and respiration rates and consequently total production. Hart and Lovvorn (2000) found that assuming a constant vertical distribution of epiphyte biomass could theoretically over- or under-estimate epiphyte community primary production (per m2 of bottom area) by up to 53%. Depth variations in photosynthetic response could further skew estimates of areal primary production as photosynthetic rates of the epiphyte layer vary with depth (Cattaneo and Kalff 1980; Kairesalo 1983; Müller 1995). Distinct types of macrophytes support variable amounts of epiphytes because of differences in plant density, architecture, leaf age, and leaf morphology (Burkholder and Wetzel 1989; Lalonde and Downing 1991; Cattaneo et al. 1998). The biomass of macrophytes and its vertical distribution in the water column influence the amount and location of colonizable surface area for epiphytes. Differing architecture among types of macrophytes results in depth variations of epiphyte 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 submerged macrophytes, the bulk of biomass is found near the surface for canopy-forming species, whereas basal rosette forms with linear leaves (such as Vallisneria americana) tend to concentrate biomass near the bottom (Westlake 1964; Titus and Adams 1979), particularly in flowing waters. The uneven distribution of macrophyte biomass in the water column also affects light intensity and quality and water movements within the stand (e.g., Westlake 1964; Van der Bijl et al. 1989; Vermaat et al. 2000), further impacting the metabolic rates of epiphyte communities. The interaction between depth and macrophyte growth form varies over time with seasonal plant growth and species succession, changing the vertical structure of macrophyte biomass distribution (Burkholder and Wetzel 1989). In early summer, macrophyte biomass is low and concentrated near the sediments. When macrophyte biomass reaches its summer peak, the plant canopy is fully developed and may occupy the entire water column. These vertical shifts in the location of the macrophyte biomass result in elevated dissolved oxygen (DO) concentrations within the canopy and reduced [DO] in the subcanopy layer in summer compared with a vertically homogeneous distribution of DO in early summer (Frodge et al. 1990). In rivers, fluctuating water levels can also result in such covariation of depth and macrophyte growth form through the concentration and expansion of macrophyte biomass in a water column of variable depth. The effects of shifts in the vertical location of macrophyte biomass on epiphyte community metabolism have received limited attention. In this study, we investigate the effects of depth and macrophyte growth form on the metabolism and areal production of epiphyte communities. Photosynthesis vs.
1015
irradiance relationships and respiration rates derived from laboratory incubations were used to calculate field rates of epiphyte primary production and respiration at various sites. Sites colonized by macrophytes with contrasting growth forms were studied over a 2-year period in Lake Saint-Pierre, a large fluvial lake of the St. Lawrence River. We first examine how epiphyte community photosynthesis and respiration vary with depth and macrophyte growth form. Secondly, we determine the influence of depth and macrophyte growth form on estimates of areal epiphyte primary production and on daily net oxygen balance (per m2 of bottom area). A 1 m drop in water levels among years provided us with the opportunity to assess the effect of the interaction between water depth and macrophyte growth form on epiphyte communities.
Materials and methods Study site Lake 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 in its water quality characteristics because of the presence of distinct water masses. Its gently sloping shores and nutrientrich waters have favoured the development of large expanses of emergent and submerged rooted aquatic vegetation (macrophytes) covering approximately 80% of the lake’s surface area (Vis et al. 2003). We sampled three sites, one within each of the major water masses, between June and October of 2000 and 2001 (Fig. 1; Table 1). Site 1, located in brown waters, rich in dissolved organic carbon (DOC) and originating principally from the Ottawa River, supported a moderate biomass of lowgrowing Vallisneria americana with a sparse canopy of Potamogeton richardsonii. Site 2, situated in relatively clear waters flowing from Lake Ontario, was colonized by Stuckenia pectinata (formerly Potamogeton pectinatus), forming a dense canopy in July, which was later succeeded by Vallisneria americana (August). Site 3 (2001 only) was under the influence of brown and heavily enriched waters of the Yamaska River. This site, located in relatively shallow water (
