Hydrobiologia (2010) 652:179–184 DOI 10.1007/s10750-010-0329-1
PRIMARY RESEARCH PAPER
Macroinvertebrate grazers, current velocity, and bedload transport rate influence periphytic accrual in a field-scale experimental stream Eric C. Merten • William D. Hintz • Anne F. Lightbody • Todd Wellnitz
Received: 4 February 2010 / Revised: 18 May 2010 / Accepted: 12 June 2010 / Published online: 26 June 2010 Ó Springer Science+Business Media B.V. 2010
Abstract Periphyton plays an important role in stream ecology, and can be sensitive to macroinvertebrate grazers, near-bed current velocity, and bedload abrasion. We manipulated conditions to examine influences on periphytic accrual in the St. Anthony Falls Laboratory Outdoor StreamLab in Minneapolis, MN, USA. Macroinvertebrate grazers were excluded from 27 of 65 clay tiles using electric pulses. We examined periphytic biomass accrual as a function of grazer presence, sampling run, and near-bed current velocity using ANCOVA. We found significant temporal differences between sampling runs but no significant effect of grazer presence. Along with a
strong association between bedload transport rates and mean periphytic biomass, our results suggest that grazers are relatively unimportant in stream systems with high levels of physical disturbance from floods and associated sand bedload. However, the interaction between grazer presence and velocity was marginally significant. Regression analyses showed no relation between velocity and periphyton in the absence of grazers but a negative relation when grazers were present, suggesting that mechanical dislodgement of periphyton by grazers may increase with velocity. We conclude that grazers can have subtle effects on periphyton, particularly in streams with high bedload transport rates. Keywords Periphyton Chlorophyll a Near-bed current velocity Bedload transport rate Experimental stream
Handling editor: L. M. Bini E. C. Merten (&) T. Wellnitz Department of Biology, University of Wisconsin—Eau Claire, 105 Garfield Ave, Eau Claire, WI 54702, USA e-mail:
[email protected] W. D. Hintz Fisheries and Illinois Aquaculture Center, Department of Zoology, Southern Illinois University, 173 Life Science II, 1125 Lincoln Dr, Carbondale, IL 62902, USA A. F. Lightbody St. Anthony Falls Laboratory, University of Minnesota, 2 Third Ave. SE, Minneapolis, MN 55414, USA
Introduction Periphyton forms an important component of stream food webs (Lamberti, 1996), and often represents the primary source of autochthonous production (Biggs, 1996). Numerous factors control periphytic biomass, including light levels, nutrients, and near-bed current velocity (Biggs & Smith, 2002; Wellnitz & Rader, 2003). Hondzo & Wang (2002), for example, showed that periphyton growth is highly dependent on the hydraulic characteristics of the benthic environment.
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In addition, sandy bedloads can change periphyton communities through abrasion (Schofield et al., 2004). Periphyton communities may be particularly altered in urban streams (Murdock et al., 2004), where anthropogenic activities can cause more flashy hydrographs and increased bedload (Gordon et al., 2004). Periphytic biomass can also be affected by macroinvertebrate grazers (Feminella & Hawkins, 1995; Opsahl et al., 2003; Liess & Hillebrand, 2004; Wellnitz & Poff, 2006). Because primary productivity can limit energy transfer to higher tropic levels, the interplay between periphyton, macroinvertebrates, and the abiotic environment has been well studied (e.g., Hayes et al., 2000; Dzialowski & Smith, 2008). For example, macroinvertebrate grazers have the potential to alter the relationship between nearbed current velocity and periphytic accrual (Opsahl et al., 2003). In the absence of grazers, periphytic accrual may be positively related to current velocity due to increased nutrient delivery, at least when periphyton are nonfilamentous and nutrient-limited (Biggs et al., 1998). At high shear stress, periphyton may become mechanically dislodged, resulting in a decrease in biomass with increasing flow velocity (Hondzo & Wang, 2002). However, when grazers are present, periphytic biomass may be negatively related to velocity, as demonstrated by Poff et al. (2003) for the grazers Baetis bicaudatus, Drunella grandis, and Glossosoma verdona. Periphytic biomass may decrease with velocity due to nonconsumptive losses (Scrimgeour et al., 1991; Catteneo & Mousseau, 1995) such as inadvertent dislodgement of periphyton by grazer activity. The goal of this study was to test two hypotheses regarding periphytic accrual, using a fieldscale experimental stream. We first hypothesized that periphytic biomass accrual would be greater in the absence of macroinvertebrate grazers. We further hypothesized that the effect of grazers on periphytic biomass would be influenced by nearbed current velocity (Biggs et al., 1998; Poff et al., 2003) as follows. In the absence of grazers, we expected periphytic biomass to increase with increasing current velocity, due to increased nutrient delivery. In the presence of grazers, we expected periphytic biomass to decrease with increasing current velocity, due to increased nonconsumptive losses.
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Methods Study area and design This study was completed in the Outdoor StreamLab,1 a field-scale experimental stream at the University of Minnesota’s St. Anthony Falls Laboratory in Minneapolis, MN, USA. The stream experienced full sunlight and ambient weather conditions, and was 40 m in length with mean bankfull width and depth of 3 and 0.16 m. The Outdoor StreamLab drew water from the Mississippi River via an inlet valve, which allowed full control of stream discharge. Sandy bedload (D50 & 0.7 mm) was distributed across the upstream end of the experimental stream area from a stockpile using a variable speed auger. The hydrograph and sedigraph were manipulated to simulate flood events with periods of high water and sediment feed separated by periods of low flow and low sediment feed (Fig. 1). Sediment feed rates were verified by periodic grab samples, which were dried for 24 h at 105°C prior to weighing. Rates were compared with the total amount of sediment exiting the stream during each sampling run, which was collected in a settling basin at the downstream end of the stream; this sediment volume was surveyed using a total station (Sokkia X30RK) and rod, subsamples of known volume were dried and weighed for bulk density determination, and the remaining sediment was stockpiled for later feed. Bedload transport rates were standardized by dividing by the bankfull width. Nitrate levels in the Outdoor StreamLab averaged 0.42 mg/l, based on samples taken in 2009 on 6/15, 7/1, 8/3, and 8/17. Phosphate samples from the Outdoor StreamLab were not available; samples from the nearest monitoring station on the Mississippi River averaged 9.3 lg/l based on samples taken on 6/15, 7/6, and 7/20 (Metropolitan Council Environmental Information Management System). During summer 2009, four sampling runs were completed: June 12–18 (run 1), June 18–July 2 (run 2), July 13–29 (run 3), and July 29–August 28 (run 4). Each run employed 17–18 unglazed clay tiles (8 9 8 9 1 cm) which were staked to the stream bed in a gravel riffle (D50 & 28 mm) to provide standardized substrates for periphytic accrual. Each
1
http://www.safl.umn.edu/facilities/OSL.html.
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Fig. 1 Water and dry weight equivalent sediment discharge into the Outdoor StreamLab during a run 1, b run 2, c run 3, and d run 4
run included eight or nine electrified tiles, which were wrapped with wire loops and connected to a Blitzer 8904 fence charger (Zareba Systems, Ellendale, MN) producing one pulse per second to exclude macroinvertebrates without directly affecting periphyton (Brown et al., 2000). The remaining nine tiles in each run were nonelectric; each was wrapped with wire loops but not connected to electricity. A MiniWater20 Micro current velocity probe (Schiltknecht Messtechnik AG, Zu¨rich, CH) was used to measure near-bed current velocity under base flow conditions at the center of each tile. Several methods were used to verify that the electric pulses did indeed exclude macroinvertebrate grazers. All tiles were inspected daily to ensure that the wires remained connected, and tests were made by hand to verify that the electric current could be felt near the electrified tiles and not the nonelectric tiles. In addition, macroinvertebrates were enumerated in situ on the surface of all tiles on ten different occasions during the study period. Student t tests were used to test for differences in the means between electrified and nonelectric tiles for total macroinvertebrates and scraping grazers. Periphytic accrual Periphytic accrual was measured on the upper surface of each tile at the end of each sampling run. The
upper side of each tile was brushed with a toothbrush and rinsed with a wash bottle. The tile was brushed and rinsed twice, followed by rinsing the toothbrush. The resulting slurry was collected, filtered through an A/E glass fiber filter, and stored in a freezer. Chlorophyll a was then extracted from the filters using ethanol saturated with MgCO3 buffer for 12–24 h in the dark. Immediately following extraction, a Trilogy fluorometer (Turner Designs, Sunnyvale, CA) was used to determine the chlorophyll a concentration on each tile, as an indicator of periphytic biomass. Seven tiles out of 65 total were omitted from analyses due to measurement problems (n = 3), complete burial by sand (n = 1), or disconnected wires (n = 3). Data analysis We tested our hypotheses using an analysis of covariance (ANCOVA). The ANCOVA used a factor for treatment (i.e., electrified or nonelectric), a factor for sampling run, a covariate for velocity, and all second-order interactions (i.e., treatment:run, treatment:velocity, and run:velocity). The response variable was periphytic accrual (via fluorometry). The fluorometry data were square-root transformed to meet assumptions of normality and homogeneity of residuals, based on the normal probability plot and residual plot. Tukey’s HSD was used to compare
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mean values for significant factors. A second ANCOVA was completed using square-root transformed fluorometry data as the response, a factor for treatment, and a covariate for mean bedload. We also used linear and nonlinear regression analyses to describe patterns in the observed data.
Results The experimental setup was successful at excluding grazers from the electrified tiles. Electrified tiles had significantly fewer total macroinvertebrates (mean ± SE 11.1 ± 1.4 and 53.3 ± 4.5, n = 166 tile counts, P \ 0.001) and scraping grazers (0.1 ± 0.05 and 1.3 ± 0.26, n = 166 tiles, P \ 0.001) than nonelectric tiles. Filter-feeding simuliids (blackfly larvae and pupae) comprised 97% of total macroinvertebrates on the tiles; grazers observed included glossosomid caddisflies (1.3%), hydroptilid caddisflies (0.6%), gastropods (0.2%), and baetid mayflies (0.1%). Hereafter we refer to electrified and nonelectric tiles as ungrazed and grazed. The main effect for grazing treatment was not significant (P = 0.21), although mean periphyton biomass on ungrazed tiles was higher than grazed tiles (126 mg/m2 vs. 98 mg/m2). Visual inspection of the tiles suggested a diatom understory with short (\0.5 cm), frequent tufts of filamentous algae. The interaction between grazing treatment and velocity was marginally significant (P = 0.08; Table 1). On ungrazed tiles, periphytic biomass was not correlated with velocity (Fig. 2A; r2 = 0.01), whereas on
grazed tiles we observed a logarithmic decline in periphytic biomass with increasing velocity (Fig. 2B; r2 = 0.63). The only other significant effect was sampling run (P \ 0.01). Tukey’s HSD on the main effect for sampling run showed that chlorophyll-a density was significantly lower (P \ 0.05) in run 3 than runs 2 or 4 (Fig. 3). Regarding the second ANCOVA, the main effect for grazing treatment was not significant (P = 0.21), the covariate for bedload was highly significant (P \ 0.01), and the interaction between grazing treatment and bedload was not significant (P = 0.29). Periphytic accrual was negatively correlated with bedload transport rates, which varied by sampling run (Fig. 4). During flood events, between 0.6 ± 0.2 and 1.0 ± 0.6 kg/m/min of sandy sediment was fed into the stream, which was primarily transported as bedload. The sediment loading was sufficient to create observable dunes even in constricted riffle areas. The relation between bedload transport rates and chlorophyll-a density on grazed tiles was stronger for grazed tiles (r2 = 0.98) than ungrazed tiles (r2 = 0.86).
Table 1 Results from an ANCOVA testing for effects of treatment (grazed or ungrazed), sampling run, and velocity on chlorophyll-a density df
Sum sq.
F value
P
Treatment
1
36
1.61
0.21
Run
3
325
4.86
\0.01
Velocity
1
21
0.95
0.34
Treatment:run
3
16
0.23
0.87
Treatment:velocity
1
69
3.11
0.08
3
129
1.93
0.14
45
1003
Run:velocity Residuals
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Fig. 2 Relationship between periphytic biomass and near-bed current velocity with grazers excluded (A) or not excluded (B)
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Fig. 3 Box-whisker plot showing quartiles and overall differences in chlorophyll a density (using fluorometry) between the four sampling runs. The mean for run 3 was significantly lower (Tukey’s HSD, P \ 0.05) than runs 2 or 4
Fig. 4 Relationship between mean bedload transport rate during each sampling run and mean chlorophyll a density (using fluorometry) for grazed and ungrazed tiles
Discussion In this study, we have demonstrated that macroinvertebrate grazers can have subtle effects on periphytic accrual, effects which may only be apparent when considered in the context of near-bed current velocity. In addition, our data showed a strong association between bedload transport rates and periphytic accrual. Conditions in the Outdoor StreamLab (i.e.,
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relatively high light availability, nutrient concentrations, and bedload transport rates) may help explain our results, and make this study more applicable to streams in urban watersheds than relatively pristine systems. Our first hypothesis was not supported, as we found no significant difference between mean periphytic biomass on grazed versus ungrazed tiles. Grazers were moderately abundant in the study riffle; Surber samples during summer 2009 showed a mean density of scraping grazers of 680/m2 in the gravel substrate surrounding the tiles (Eric Merten, unpublished data). Although, previous studies have shown that grazers may enhance algal growth (Wellnitz & Poff, 2006), a decrease is much more common (Feminella & Hawkins, 1995; Liess & Hillebrand, 2004). One possible explanation for the lack of a grazing effect was that the abundant simuliids inhibited grazing activity via competition for space on the tiles, although we did not attempt to observe such interactions. Despite the presence of grazers, bedload abrasion may have masked their effects on periphytic accrual. Although duration (and possibly nutrients) also varied between runs, the data suggest a direct influence of bedload. The hydrograph and sedigraph were particularly variable during run 3, the run with the lowest mean periphytic biomass. Our data from the Outdoor StreamLab support the contention by Schofield et al. (2004) that grazing is relatively unimportant under conditions of high bedload transport. Although they did not exclude grazers, Murdock et al. (2004) similarly concluded that abiotic forces (e.g., sloughing and abrasion) were more important to periphyton in urban streams than grazers. Our second hypothesis was partially supported; grazed and ungrazed tiles did have different relationships between periphytic biomass and near-bed current velocity. Ungrazed tiles showed no relation between periphytic biomass and velocity, suggesting that other abiotic factors (e.g., bedload transport rates or duration of the sampling run) were more important than nutrient delivery. Nutrient levels in the Mississippi River water feeding the Outdoor StreamLab may not have limited periphyton growth. Grazed tiles, however, showed a negative relation between near-bed current velocity and periphyton accrual, consistent with the results of Opsahl et al. (2003). Nonconsumptive loss (Scrimgeour et al., 1991; Cattaneo & Mousseau, 1995), particularly periphyton
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dislodgement at faster velocities by the physical activity of grazers or other macroinvertebrates, is certainly a possible explanation, analogous to greater detachment of filamentous algae under higher shear stresses (Biggs et al., 1998). In conclusion, experimental streams such as the Outdoor StreamLab provide a unique opportunity to examine periphyton dynamics under controlled conditions. Research in relatively pristine systems (Opsahl et al., 2003) has shown a more direct role of grazers, but our study demonstrated that grazers can have subtle effects in flashy, sand-dominated streams. The fluctuating hydrograph and sandy bedload during our study may not be uncommon in storm-driven systems, particularly in urban areas (Gordon et al., 2004). As such, bedload abrasion may be a more important driver of periphyton accrual than has generally been recognized (Schofield et al., 2004). Acknowledgments Kathryn Kramarczuk provided technical assistance and an ongoing presence at the Outdoor StreamLab which made this work possible. Mallory Immerfall, Jordan Theissen, and Brandon Trimbell also assisted with experimental setup and maintenance. Miki Hondzo gave advice on the experimental design. This work was supported by the National Science Foundation through a CAREER grant (DEB-0642512) to T.W. and by the STC program via the National Center for Earth-surface Dynamics under agreement number EAR-0120914.
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